diff --git a/zebra-network/src/peer_set/initialize.rs b/zebra-network/src/peer_set/initialize.rs
index d01a6a314..ab355b6fc 100644
--- a/zebra-network/src/peer_set/initialize.rs
+++ b/zebra-network/src/peer_set/initialize.rs
@@ -144,6 +144,7 @@ where
 
     // Connect the rx end to a PeerSet, wrapping new peers in load instruments.
     let peer_set = PeerSet::new(
+        &config,
         PeakEwmaDiscover::new(
             // Discover interprets an error as stream termination,
             // so discard any errored connections...
@@ -162,19 +163,20 @@ where
     // Connect peerset_tx to the 3 peer sources:
     //
     // 1. Incoming peer connections, via a listener.
-    let listen_guard = tokio::spawn(
-        accept_inbound_connections(tcp_listener, listen_handshaker, peerset_tx.clone())
-            .instrument(Span::current()),
+    let listen_fut = accept_inbound_connections(
+        config.clone(),
+        tcp_listener,
+        listen_handshaker,
+        peerset_tx.clone(),
     );
+    let listen_guard = tokio::spawn(listen_fut.instrument(Span::current()));
 
     // 2. Initial peers, specified in the config.
-    let initial_peers_fut = {
-        let config = config.clone();
-        let outbound_connector = outbound_connector.clone();
-        let peerset_tx = peerset_tx.clone();
-        add_initial_peers(config, outbound_connector, peerset_tx)
-    };
-
+    let initial_peers_fut = add_initial_peers(
+        config.clone(),
+        outbound_connector.clone(),
+        peerset_tx.clone(),
+    );
     let initial_peers_join = tokio::spawn(initial_peers_fut.instrument(Span::current()));
 
     // 3. Outgoing peers we connect to in response to load.
@@ -202,18 +204,15 @@ where
         let _ = demand_tx.try_send(MorePeers);
     }
 
-    let crawl_fut = {
-        let config = config.clone();
-        crawl_and_dial(
-            config,
-            demand_tx,
-            demand_rx,
-            candidates,
-            outbound_connector,
-            peerset_tx,
-            active_outbound_connections,
-        )
-    };
+    let crawl_fut = crawl_and_dial(
+        config,
+        demand_tx,
+        demand_rx,
+        candidates,
+        outbound_connector,
+        peerset_tx,
+        active_outbound_connections,
+    );
     let crawl_guard = tokio::spawn(crawl_fut.instrument(Span::current()));
 
     handle_tx.send(vec![listen_guard, crawl_guard]).unwrap();
@@ -434,8 +433,11 @@ async fn open_listener(config: &Config) -> (TcpListener, SocketAddr) {
 ///
 /// Uses `handshaker` to perform a Zcash network protocol handshake, and sends
 /// the [`peer::Client`] result over `peerset_tx`.
-#[instrument(skip(listener, handshaker, peerset_tx), fields(listener_addr = ?listener.local_addr()))]
+///
+/// Limit the number of active inbound connections based on `config`.
+#[instrument(skip(config, listener, handshaker, peerset_tx), fields(listener_addr = ?listener.local_addr()))]
 async fn accept_inbound_connections<S>(
+    config: Config,
     listener: TcpListener,
     mut handshaker: S,
     peerset_tx: mpsc::Sender<PeerChange>,
@@ -447,8 +449,19 @@ where
     let mut active_inbound_connections = ActiveConnectionCounter::new_counter();
 
     loop {
-        if let Ok((tcp_stream, addr)) = listener.accept().await {
-            // The peer already opened a connection, so increment the connection count immediately.
+        let inbound_result = listener.accept().await;
+        if let Ok((tcp_stream, addr)) = inbound_result {
+            if active_inbound_connections.update_count()
+                >= config.peerset_inbound_connection_limit()
+            {
+                // Too many open inbound connections or pending handshakes already.
+                // Close the connection.
+                std::mem::drop(tcp_stream);
+                continue;
+            }
+
+            // The peer already opened a connection to us.
+            // So we want to increment the connection count as soon as possible.
             let connection_tracker = active_inbound_connections.track_connection();
             debug!(
                 inbound_connections = ?active_inbound_connections.update_count(),
@@ -492,6 +505,8 @@ where
             // Zebra can't control how many queued connections are waiting,
             // but most OSes also limit the number of queued inbound connections on a listener port.
             tokio::time::sleep(constants::MIN_PEER_CONNECTION_INTERVAL).await;
+        } else {
+            debug!(?inbound_result, "error accepting inbound connection");
         }
 
         // Security: Let other tasks run after each connection is processed.
@@ -536,8 +551,8 @@ enum CrawlerAction {
 /// permanent internal error. Transient errors and individual peer errors should
 /// be handled within the crawler.
 ///
-/// Uses `active_outbound_connections` to track the number of active outbound connections
-/// in both the initial peers and crawler.
+/// Uses `active_outbound_connections` to limit the number of active outbound connections
+/// across both the initial peers and crawler. The limit is based on `config`.
 #[instrument(skip(
     config,
     demand_tx,
@@ -606,7 +621,7 @@ where
             // turn the demand into an action, based on the crawler's current state
             _ = demand_rx.next() => {
                 if active_outbound_connections.update_count() >= config.peerset_outbound_connection_limit() {
-                    // Too many open connections or pending handshakes already
+                    // Too many open outbound connections or pending handshakes already
                     DemandDrop
                 } else if let Some(candidate) = candidates.next().await {
                     // candidates.next has a short delay, and briefly holds the address
diff --git a/zebra-network/src/peer_set/initialize/tests/vectors.rs b/zebra-network/src/peer_set/initialize/tests/vectors.rs
index 71366de8a..245fb212b 100644
--- a/zebra-network/src/peer_set/initialize/tests/vectors.rs
+++ b/zebra-network/src/peer_set/initialize/tests/vectors.rs
@@ -24,7 +24,7 @@ use futures::{
     channel::{mpsc, oneshot},
     FutureExt, StreamExt,
 };
-use tokio::task::JoinHandle;
+use tokio::{net::TcpStream, task::JoinHandle};
 use tower::{discover::Change, service_fn, Service};
 use tracing::Span;
 
@@ -34,9 +34,12 @@ use zebra_test::net::random_known_port;
 use crate::{
     constants, init,
     meta_addr::MetaAddr,
-    peer::{self, ErrorSlot, OutboundConnectorRequest},
+    peer::{self, ErrorSlot, HandshakeRequest, OutboundConnectorRequest},
     peer_set::{
-        initialize::{add_initial_peers, crawl_and_dial, PeerChange},
+        initialize::{
+            accept_inbound_connections, add_initial_peers, crawl_and_dial, open_listener,
+            PeerChange,
+        },
         set::MorePeers,
         ActiveConnectionCounter, CandidateSet,
     },
@@ -51,12 +54,17 @@ use Network::*;
 /// Using a very short time can make the crawler not run at all.
 const CRAWLER_TEST_DURATION: Duration = Duration::from_secs(10);
 
+/// The amount of time to run the listener, before testing what it has done.
+///
+/// Using a very short time can make the listener not run at all.
+const LISTENER_TEST_DURATION: Duration = Duration::from_secs(10);
+
 /// Test that zebra-network discovers dynamic bind-to-all-interfaces listener ports,
 /// and sends them to the `AddressBook`.
 ///
 /// Note: This test doesn't cover local interface or public IP address discovery.
 #[tokio::test]
-async fn local_listener_unspecified_port_unspecified_addr() {
+async fn local_listener_unspecified_port_unspecified_addr_v4() {
     zebra_test::init();
 
     if zebra_test::net::zebra_skip_network_tests() {
@@ -67,6 +75,19 @@ async fn local_listener_unspecified_port_unspecified_addr() {
     // (localhost should be enough)
     local_listener_port_with("0.0.0.0:0".parse().unwrap(), Mainnet).await;
     local_listener_port_with("0.0.0.0:0".parse().unwrap(), Testnet).await;
+}
+
+/// Test that zebra-network discovers dynamic bind-to-all-interfaces listener ports,
+/// and sends them to the `AddressBook`.
+///
+/// Note: This test doesn't cover local interface or public IP address discovery.
+#[tokio::test]
+async fn local_listener_unspecified_port_unspecified_addr_v6() {
+    zebra_test::init();
+
+    if zebra_test::net::zebra_skip_network_tests() {
+        return;
+    }
 
     if zebra_test::net::zebra_skip_ipv6_tests() {
         return;
@@ -80,7 +101,7 @@ async fn local_listener_unspecified_port_unspecified_addr() {
 /// Test that zebra-network discovers dynamic localhost listener ports,
 /// and sends them to the `AddressBook`.
 #[tokio::test]
-async fn local_listener_unspecified_port_localhost_addr() {
+async fn local_listener_unspecified_port_localhost_addr_v4() {
     zebra_test::init();
 
     if zebra_test::net::zebra_skip_network_tests() {
@@ -90,6 +111,17 @@ async fn local_listener_unspecified_port_localhost_addr() {
     // these tests might fail on machines with unusual IPv4 localhost configs
     local_listener_port_with("127.0.0.1:0".parse().unwrap(), Mainnet).await;
     local_listener_port_with("127.0.0.1:0".parse().unwrap(), Testnet).await;
+}
+
+/// Test that zebra-network discovers dynamic localhost listener ports,
+/// and sends them to the `AddressBook`.
+#[tokio::test]
+async fn local_listener_unspecified_port_localhost_addr_v6() {
+    zebra_test::init();
+
+    if zebra_test::net::zebra_skip_network_tests() {
+        return;
+    }
 
     if zebra_test::net::zebra_skip_ipv6_tests() {
         return;
@@ -102,11 +134,10 @@ async fn local_listener_unspecified_port_localhost_addr() {
 
 /// Test that zebra-network propagates fixed localhost listener ports to the `AddressBook`.
 #[tokio::test]
-async fn local_listener_fixed_port_localhost_addr() {
+async fn local_listener_fixed_port_localhost_addr_v4() {
     zebra_test::init();
 
     let localhost_v4 = "127.0.0.1".parse().unwrap();
-    let localhost_v6 = "::1".parse().unwrap();
 
     if zebra_test::net::zebra_skip_network_tests() {
         return;
@@ -114,6 +145,18 @@ async fn local_listener_fixed_port_localhost_addr() {
 
     local_listener_port_with(SocketAddr::new(localhost_v4, random_known_port()), Mainnet).await;
     local_listener_port_with(SocketAddr::new(localhost_v4, random_known_port()), Testnet).await;
+}
+
+/// Test that zebra-network propagates fixed localhost listener ports to the `AddressBook`.
+#[tokio::test]
+async fn local_listener_fixed_port_localhost_addr_v6() {
+    zebra_test::init();
+
+    let localhost_v6 = "::1".parse().unwrap();
+
+    if zebra_test::net::zebra_skip_network_tests() {
+        return;
+    }
 
     if zebra_test::net::zebra_skip_ipv6_tests() {
         return;
@@ -253,10 +296,10 @@ async fn crawler_peer_limit_zero_connect_panic() {
         unreachable!("outbound connector should never be called with a zero peer limit")
     });
 
-    let (_config, mut peerset_tx) =
+    let (_config, mut peerset_rx) =
         spawn_crawler_with_peer_limit(0, unreachable_outbound_connector).await;
 
-    let peer_result = peerset_tx.try_next();
+    let peer_result = peerset_rx.try_next();
     assert!(
         // `Err(_)` means that no peers are available, and the sender has not been dropped.
         // `Ok(None)` means that no peers are available, and the sender has been dropped.
@@ -277,10 +320,10 @@ async fn crawler_peer_limit_one_connect_error() {
     let error_outbound_connector =
         service_fn(|_| async { Err("test outbound connector always returns errors".into()) });
 
-    let (_config, mut peerset_tx) =
+    let (_config, mut peerset_rx) =
         spawn_crawler_with_peer_limit(1, error_outbound_connector).await;
 
-    let peer_result = peerset_tx.try_next();
+    let peer_result = peerset_rx.try_next();
     assert!(
         // `Err(_)` means that no peers are available, and the sender has not been dropped.
         // `Ok(None)` means that no peers are available, and the sender has been dropped.
@@ -325,12 +368,12 @@ async fn crawler_peer_limit_one_connect_ok_then_drop() {
             Ok(Change::Insert(addr, fake_client))
         });
 
-    let (config, mut peerset_tx) =
+    let (config, mut peerset_rx) =
         spawn_crawler_with_peer_limit(1, success_disconnect_outbound_connector).await;
 
     let mut peer_count: usize = 0;
     loop {
-        let peer_result = peerset_tx.try_next();
+        let peer_result = peerset_rx.try_next();
         match peer_result {
             // A peer handshake succeeded.
             Ok(Some(peer_result)) => {
@@ -368,8 +411,11 @@ async fn crawler_peer_limit_one_connect_ok_stay_open() {
     // This test does not require network access, because the outbound connector
     // and peer set are fake.
 
-    let success_stay_open_outbound_connector =
-        service_fn(|req: OutboundConnectorRequest| async move {
+    let (peer_tracker_tx, mut peer_tracker_rx) = mpsc::unbounded();
+
+    let success_stay_open_outbound_connector = service_fn(move |req: OutboundConnectorRequest| {
+        let peer_tracker_tx = peer_tracker_tx.clone();
+        async move {
             let OutboundConnectorRequest {
                 addr,
                 connection_tracker,
@@ -385,29 +431,49 @@ async fn crawler_peer_limit_one_connect_ok_stay_open() {
                 error_slot,
             };
 
-            // Fake the connection being open forever.
-            std::mem::forget(connection_tracker);
+            // Make the connection staying open.
+            peer_tracker_tx
+                .unbounded_send(connection_tracker)
+                .expect("unexpected error sending to unbounded channel");
 
             Ok(Change::Insert(addr, fake_client))
-        });
+        }
+    });
 
-    let (config, mut peerset_tx) =
+    let (config, mut peerset_rx) =
         spawn_crawler_with_peer_limit(1, success_stay_open_outbound_connector).await;
 
-    let mut peer_count: usize = 0;
+    let mut peer_change_count: usize = 0;
     loop {
-        let peer_result = peerset_tx.try_next();
-        match peer_result {
+        let peer_change_result = peerset_rx.try_next();
+        match peer_change_result {
             // A peer handshake succeeded.
-            Ok(Some(peer_result)) => {
+            Ok(Some(peer_change_result)) => {
                 assert!(
-                    matches!(peer_result, Ok(Change::Insert(_, _))),
+                    matches!(peer_change_result, Ok(Change::Insert(_, _))),
                     "unexpected connection error: {:?}\n\
                      {} previous peers succeeded",
-                    peer_result,
-                    peer_count,
+                    peer_change_result,
+                    peer_change_count,
                 );
-                peer_count += 1;
+                peer_change_count += 1;
+            }
+
+            // The channel is closed and there are no messages left in the channel.
+            Ok(None) => break,
+            // The channel is still open, but there are no messages left in the channel.
+            Err(_) => break,
+        }
+    }
+
+    let mut peer_tracker_count: usize = 0;
+    loop {
+        let peer_tracker_result = peer_tracker_rx.try_next();
+        match peer_tracker_result {
+            // We held this peer tracker open until now.
+            Ok(Some(peer_tracker)) => {
+                std::mem::drop(peer_tracker);
+                peer_tracker_count += 1;
             }
 
             // The channel is closed and there are no messages left in the channel.
@@ -418,10 +484,19 @@ async fn crawler_peer_limit_one_connect_ok_stay_open() {
     }
 
     assert!(
-        peer_count <= config.peerset_outbound_connection_limit(),
-        "unexpected number of peer connections {}, over limit of {}",
-        peer_count,
+        peer_change_count <= config.peerset_outbound_connection_limit(),
+        "unexpected number of peer changes {}, over limit of {}, had {} peer trackers",
+        peer_change_count,
         config.peerset_outbound_connection_limit(),
+        peer_tracker_count,
+    );
+
+    assert!(
+        peer_tracker_count <= config.peerset_outbound_connection_limit(),
+        "unexpected number of peer trackers {}, over limit of {}, had {} peer changes",
+        peer_tracker_count,
+        config.peerset_outbound_connection_limit(),
+        peer_change_count,
     );
 }
 
@@ -436,10 +511,10 @@ async fn crawler_peer_limit_default_connect_error() {
     let error_outbound_connector =
         service_fn(|_| async { Err("test outbound connector always returns errors".into()) });
 
-    let (_config, mut peerset_tx) =
+    let (_config, mut peerset_rx) =
         spawn_crawler_with_peer_limit(None, error_outbound_connector).await;
 
-    let peer_result = peerset_tx.try_next();
+    let peer_result = peerset_rx.try_next();
     assert!(
         // `Err(_)` means that no peers are available, and the sender has not been dropped.
         // `Ok(None)` means that no peers are available, and the sender has been dropped.
@@ -484,12 +559,14 @@ async fn crawler_peer_limit_default_connect_ok_then_drop() {
             Ok(Change::Insert(addr, fake_client))
         });
 
-    let (config, mut peerset_tx) =
-        spawn_crawler_with_peer_limit(None, success_disconnect_outbound_connector).await;
+    // TODO: tweak the crawler timeouts and rate-limits so we get over the actual limit
+    //       (currently, getting over the limit can take 30 seconds or more)
+    let (config, mut peerset_rx) =
+        spawn_crawler_with_peer_limit(15, success_disconnect_outbound_connector).await;
 
     let mut peer_count: usize = 0;
     loop {
-        let peer_result = peerset_tx.try_next();
+        let peer_result = peerset_rx.try_next();
         match peer_result {
             // A peer handshake succeeded.
             Ok(Some(peer_result)) => {
@@ -510,14 +587,11 @@ async fn crawler_peer_limit_default_connect_ok_then_drop() {
         }
     }
 
-    // TODO: tweak the crawler timeouts and rate-limits so we get over the actual limit
-    //       (currently, getting over the limit can take 30 seconds or more)
-    let lower_limit = config.peerset_outbound_connection_limit() / 3;
     assert!(
-        peer_count > lower_limit,
+        peer_count > config.peerset_outbound_connection_limit(),
         "unexpected number of peer connections {}, should be over the limit of {}",
         peer_count,
-        lower_limit,
+        config.peerset_outbound_connection_limit(),
     );
 }
 
@@ -530,8 +604,11 @@ async fn crawler_peer_limit_default_connect_ok_stay_open() {
     // This test does not require network access, because the outbound connector
     // and peer set are fake.
 
-    let success_stay_open_outbound_connector =
-        service_fn(|req: OutboundConnectorRequest| async move {
+    let (peer_tracker_tx, mut peer_tracker_rx) = mpsc::unbounded();
+
+    let success_stay_open_outbound_connector = service_fn(move |req: OutboundConnectorRequest| {
+        let peer_tracker_tx = peer_tracker_tx.clone();
+        async move {
             let OutboundConnectorRequest {
                 addr,
                 connection_tracker,
@@ -547,19 +624,173 @@ async fn crawler_peer_limit_default_connect_ok_stay_open() {
                 error_slot,
             };
 
-            // Fake the connection being open forever.
-            std::mem::forget(connection_tracker);
+            // Make the connection staying open.
+            peer_tracker_tx
+                .unbounded_send(connection_tracker)
+                .expect("unexpected error sending to unbounded channel");
 
             Ok(Change::Insert(addr, fake_client))
-        });
+        }
+    });
 
     // The initial target size is multiplied by 1.5 to give the actual limit.
-    let (config, mut peerset_tx) =
+    let (config, mut peerset_rx) =
         spawn_crawler_with_peer_limit(None, success_stay_open_outbound_connector).await;
 
+    let mut peer_change_count: usize = 0;
+    loop {
+        let peer_change_result = peerset_rx.try_next();
+        match peer_change_result {
+            // A peer handshake succeeded.
+            Ok(Some(peer_change_result)) => {
+                assert!(
+                    matches!(peer_change_result, Ok(Change::Insert(_, _))),
+                    "unexpected connection error: {:?}\n\
+                     {} previous peers succeeded",
+                    peer_change_result,
+                    peer_change_count,
+                );
+                peer_change_count += 1;
+            }
+
+            // The channel is closed and there are no messages left in the channel.
+            Ok(None) => break,
+            // The channel is still open, but there are no messages left in the channel.
+            Err(_) => break,
+        }
+    }
+
+    let mut peer_tracker_count: usize = 0;
+    loop {
+        let peer_tracker_result = peer_tracker_rx.try_next();
+        match peer_tracker_result {
+            // We held this peer tracker open until now.
+            Ok(Some(peer_tracker)) => {
+                std::mem::drop(peer_tracker);
+                peer_tracker_count += 1;
+            }
+
+            // The channel is closed and there are no messages left in the channel.
+            Ok(None) => break,
+            // The channel is still open, but there are no messages left in the channel.
+            Err(_) => break,
+        }
+    }
+
+    assert!(
+        peer_change_count <= config.peerset_outbound_connection_limit(),
+        "unexpected number of peer changes {}, over limit of {}, had {} peer trackers",
+        peer_change_count,
+        config.peerset_outbound_connection_limit(),
+        peer_tracker_count,
+    );
+
+    assert!(
+        peer_tracker_count <= config.peerset_outbound_connection_limit(),
+        "unexpected number of peer trackers {}, over limit of {}, had {} peer changes",
+        peer_tracker_count,
+        config.peerset_outbound_connection_limit(),
+        peer_change_count,
+    );
+}
+
+/// Test the listener with an inbound peer limit of zero peers, and a handshaker that panics.
+#[tokio::test]
+async fn listener_peer_limit_zero_handshake_panic() {
+    zebra_test::init();
+
+    // This test requires an IPv4 network stack with 127.0.0.1 as localhost.
+    if zebra_test::net::zebra_skip_network_tests() {
+        return;
+    }
+
+    let unreachable_inbound_handshaker = service_fn(|_| async {
+        unreachable!("inbound handshaker should never be called with a zero peer limit")
+    });
+
+    let (_config, mut peerset_rx) =
+        spawn_inbound_listener_with_peer_limit(0, unreachable_inbound_handshaker).await;
+
+    let peer_result = peerset_rx.try_next();
+    assert!(
+        // `Err(_)` means that no peers are available, and the sender has not been dropped.
+        // `Ok(None)` means that no peers are available, and the sender has been dropped.
+        matches!(peer_result, Err(_) | Ok(None)),
+        "unexpected peer when inbound limit is zero: {:?}",
+        peer_result,
+    );
+}
+
+/// Test the listener with an inbound peer limit of one peer, and a handshaker that always errors.
+#[tokio::test]
+async fn listener_peer_limit_one_handshake_error() {
+    zebra_test::init();
+
+    // This test requires an IPv4 network stack with 127.0.0.1 as localhost.
+    if zebra_test::net::zebra_skip_network_tests() {
+        return;
+    }
+
+    let error_inbound_handshaker =
+        service_fn(|_| async { Err("test inbound handshaker always returns errors".into()) });
+
+    let (_config, mut peerset_rx) =
+        spawn_inbound_listener_with_peer_limit(1, error_inbound_handshaker).await;
+
+    let peer_result = peerset_rx.try_next();
+    assert!(
+        // `Err(_)` means that no peers are available, and the sender has not been dropped.
+        // `Ok(None)` means that no peers are available, and the sender has been dropped.
+        matches!(peer_result, Err(_) | Ok(None)),
+        "unexpected peer when all handshakes error: {:?}",
+        peer_result,
+    );
+}
+
+/// Test the listener with an inbound peer limit of one peer,
+/// and a handshaker that returns success then disconnects the peer.
+#[tokio::test]
+async fn listener_peer_limit_one_handshake_ok_then_drop() {
+    zebra_test::init();
+
+    // This test requires an IPv4 network stack with 127.0.0.1 as localhost.
+    if zebra_test::net::zebra_skip_network_tests() {
+        return;
+    }
+
+    let success_disconnect_inbound_handshaker = service_fn(|req: HandshakeRequest| async move {
+        let HandshakeRequest {
+            tcp_stream,
+            connected_addr: _,
+            connection_tracker,
+        } = req;
+
+        let (server_tx, _server_rx) = mpsc::channel(0);
+        let (shutdown_tx, _shutdown_rx) = oneshot::channel();
+        let error_slot = ErrorSlot::default();
+
+        let fake_client = peer::Client {
+            shutdown_tx: Some(shutdown_tx),
+            server_tx,
+            error_slot,
+        };
+
+        // Actually close the connection.
+        std::mem::drop(connection_tracker);
+        std::mem::drop(tcp_stream);
+
+        // Give the crawler time to get the message.
+        tokio::task::yield_now().await;
+
+        Ok(fake_client)
+    });
+
+    let (config, mut peerset_rx) =
+        spawn_inbound_listener_with_peer_limit(1, success_disconnect_inbound_handshaker).await;
+
     let mut peer_count: usize = 0;
     loop {
-        let peer_result = peerset_tx.try_next();
+        let peer_result = peerset_rx.try_next();
         match peer_result {
             // A peer handshake succeeded.
             Ok(Some(peer_result)) => {
@@ -581,10 +812,312 @@ async fn crawler_peer_limit_default_connect_ok_stay_open() {
     }
 
     assert!(
-        peer_count <= config.peerset_outbound_connection_limit(),
-        "unexpected number of peer connections {}, over limit of {}",
+        peer_count > config.peerset_inbound_connection_limit(),
+        "unexpected number of peer connections {}, should be over the limit of {}",
         peer_count,
-        config.peerset_outbound_connection_limit(),
+        config.peerset_inbound_connection_limit(),
+    );
+}
+
+/// Test the listener with an inbound peer limit of one peer,
+/// and a handshaker that returns success then holds the peer open.
+#[tokio::test]
+async fn listener_peer_limit_one_handshake_ok_stay_open() {
+    zebra_test::init();
+
+    // This test requires an IPv4 network stack with 127.0.0.1 as localhost.
+    if zebra_test::net::zebra_skip_network_tests() {
+        return;
+    }
+
+    let (peer_tracker_tx, mut peer_tracker_rx) = mpsc::unbounded();
+
+    let success_stay_open_inbound_handshaker = service_fn(move |req: HandshakeRequest| {
+        let peer_tracker_tx = peer_tracker_tx.clone();
+        async move {
+            let HandshakeRequest {
+                tcp_stream,
+                connected_addr: _,
+                connection_tracker,
+            } = req;
+
+            let (server_tx, _server_rx) = mpsc::channel(0);
+            let (shutdown_tx, _shutdown_rx) = oneshot::channel();
+            let error_slot = ErrorSlot::default();
+
+            let fake_client = peer::Client {
+                shutdown_tx: Some(shutdown_tx),
+                server_tx,
+                error_slot,
+            };
+
+            // Make the connection staying open.
+            peer_tracker_tx
+                .unbounded_send((tcp_stream, connection_tracker))
+                .expect("unexpected error sending to unbounded channel");
+
+            Ok(fake_client)
+        }
+    });
+
+    let (config, mut peerset_rx) =
+        spawn_inbound_listener_with_peer_limit(1, success_stay_open_inbound_handshaker).await;
+
+    let mut peer_change_count: usize = 0;
+    loop {
+        let peer_change_result = peerset_rx.try_next();
+        match peer_change_result {
+            // A peer handshake succeeded.
+            Ok(Some(peer_change_result)) => {
+                assert!(
+                    matches!(peer_change_result, Ok(Change::Insert(_, _))),
+                    "unexpected connection error: {:?}\n\
+                     {} previous peers succeeded",
+                    peer_change_result,
+                    peer_change_count,
+                );
+                peer_change_count += 1;
+            }
+
+            // The channel is closed and there are no messages left in the channel.
+            Ok(None) => break,
+            // The channel is still open, but there are no messages left in the channel.
+            Err(_) => break,
+        }
+    }
+
+    let mut peer_tracker_count: usize = 0;
+    loop {
+        let peer_tracker_result = peer_tracker_rx.try_next();
+        match peer_tracker_result {
+            // We held this peer connection and tracker open until now.
+            Ok(Some((peer_connection, peer_tracker))) => {
+                std::mem::drop(peer_connection);
+                std::mem::drop(peer_tracker);
+                peer_tracker_count += 1;
+            }
+
+            // The channel is closed and there are no messages left in the channel.
+            Ok(None) => break,
+            // The channel is still open, but there are no messages left in the channel.
+            Err(_) => break,
+        }
+    }
+
+    assert!(
+        peer_change_count <= config.peerset_inbound_connection_limit(),
+        "unexpected number of peer changes {}, over limit of {}, had {} peer trackers",
+        peer_change_count,
+        config.peerset_inbound_connection_limit(),
+        peer_tracker_count,
+    );
+
+    assert!(
+        peer_tracker_count <= config.peerset_inbound_connection_limit(),
+        "unexpected number of peer trackers {}, over limit of {}, had {} peer changes",
+        peer_tracker_count,
+        config.peerset_inbound_connection_limit(),
+        peer_change_count,
+    );
+}
+
+/// Test the listener with the default inbound peer limit, and a handshaker that always errors.
+#[tokio::test]
+async fn listener_peer_limit_default_handshake_error() {
+    zebra_test::init();
+
+    // This test requires an IPv4 network stack with 127.0.0.1 as localhost.
+    if zebra_test::net::zebra_skip_network_tests() {
+        return;
+    }
+
+    let error_inbound_handshaker =
+        service_fn(|_| async { Err("test inbound handshaker always returns errors".into()) });
+
+    let (_config, mut peerset_rx) =
+        spawn_inbound_listener_with_peer_limit(None, error_inbound_handshaker).await;
+
+    let peer_result = peerset_rx.try_next();
+    assert!(
+        // `Err(_)` means that no peers are available, and the sender has not been dropped.
+        // `Ok(None)` means that no peers are available, and the sender has been dropped.
+        matches!(peer_result, Err(_) | Ok(None)),
+        "unexpected peer when all handshakes error: {:?}",
+        peer_result,
+    );
+}
+
+/// Test the listener with the default inbound peer limit,
+/// and a handshaker that returns success then disconnects the peer.
+#[tokio::test]
+async fn listener_peer_limit_default_handshake_ok_then_drop() {
+    zebra_test::init();
+
+    // This test requires an IPv4 network stack with 127.0.0.1 as localhost.
+    if zebra_test::net::zebra_skip_network_tests() {
+        return;
+    }
+
+    let success_disconnect_inbound_handshaker = service_fn(|req: HandshakeRequest| async move {
+        let HandshakeRequest {
+            tcp_stream,
+            connected_addr: _,
+            connection_tracker,
+        } = req;
+
+        let (server_tx, _server_rx) = mpsc::channel(0);
+        let (shutdown_tx, _shutdown_rx) = oneshot::channel();
+        let error_slot = ErrorSlot::default();
+
+        let fake_client = peer::Client {
+            shutdown_tx: Some(shutdown_tx),
+            server_tx,
+            error_slot,
+        };
+
+        // Actually close the connection.
+        std::mem::drop(connection_tracker);
+        std::mem::drop(tcp_stream);
+
+        // Give the crawler time to get the message.
+        tokio::task::yield_now().await;
+
+        Ok(fake_client)
+    });
+
+    let (config, mut peerset_rx) =
+        spawn_inbound_listener_with_peer_limit(None, success_disconnect_inbound_handshaker).await;
+
+    let mut peer_count: usize = 0;
+    loop {
+        let peer_result = peerset_rx.try_next();
+        match peer_result {
+            // A peer handshake succeeded.
+            Ok(Some(peer_result)) => {
+                assert!(
+                    matches!(peer_result, Ok(Change::Insert(_, _))),
+                    "unexpected connection error: {:?}\n\
+                     {} previous peers succeeded",
+                    peer_result,
+                    peer_count,
+                );
+                peer_count += 1;
+            }
+
+            // The channel is closed and there are no messages left in the channel.
+            Ok(None) => break,
+            // The channel is still open, but there are no messages left in the channel.
+            Err(_) => break,
+        }
+    }
+
+    assert!(
+        peer_count > config.peerset_inbound_connection_limit(),
+        "unexpected number of peer connections {}, should be over the limit of {}",
+        peer_count,
+        config.peerset_inbound_connection_limit(),
+    );
+}
+
+/// Test the listener with the default inbound peer limit,
+/// and a handshaker that returns success then holds the peer open.
+#[tokio::test]
+async fn listener_peer_limit_default_handshake_ok_stay_open() {
+    zebra_test::init();
+
+    // This test requires an IPv4 network stack with 127.0.0.1 as localhost.
+    if zebra_test::net::zebra_skip_network_tests() {
+        return;
+    }
+
+    let (peer_tracker_tx, mut peer_tracker_rx) = mpsc::unbounded();
+
+    let success_stay_open_inbound_handshaker = service_fn(move |req: HandshakeRequest| {
+        let peer_tracker_tx = peer_tracker_tx.clone();
+        async move {
+            let HandshakeRequest {
+                tcp_stream,
+                connected_addr: _,
+                connection_tracker,
+            } = req;
+
+            let (server_tx, _server_rx) = mpsc::channel(0);
+            let (shutdown_tx, _shutdown_rx) = oneshot::channel();
+            let error_slot = ErrorSlot::default();
+
+            let fake_client = peer::Client {
+                shutdown_tx: Some(shutdown_tx),
+                server_tx,
+                error_slot,
+            };
+
+            // Make the connection staying open.
+            peer_tracker_tx
+                .unbounded_send((tcp_stream, connection_tracker))
+                .expect("unexpected error sending to unbounded channel");
+
+            Ok(fake_client)
+        }
+    });
+
+    let (config, mut peerset_rx) =
+        spawn_inbound_listener_with_peer_limit(None, success_stay_open_inbound_handshaker).await;
+
+    let mut peer_change_count: usize = 0;
+    loop {
+        let peer_change_result = peerset_rx.try_next();
+        match peer_change_result {
+            // A peer handshake succeeded.
+            Ok(Some(peer_change_result)) => {
+                assert!(
+                    matches!(peer_change_result, Ok(Change::Insert(_, _))),
+                    "unexpected connection error: {:?}\n\
+                     {} previous peers succeeded",
+                    peer_change_result,
+                    peer_change_count,
+                );
+                peer_change_count += 1;
+            }
+
+            // The channel is closed and there are no messages left in the channel.
+            Ok(None) => break,
+            // The channel is still open, but there are no messages left in the channel.
+            Err(_) => break,
+        }
+    }
+
+    let mut peer_tracker_count: usize = 0;
+    loop {
+        let peer_tracker_result = peer_tracker_rx.try_next();
+        match peer_tracker_result {
+            // We held this peer connection and tracker open until now.
+            Ok(Some((peer_connection, peer_tracker))) => {
+                std::mem::drop(peer_connection);
+                std::mem::drop(peer_tracker);
+                peer_tracker_count += 1;
+            }
+
+            // The channel is closed and there are no messages left in the channel.
+            Ok(None) => break,
+            // The channel is still open, but there are no messages left in the channel.
+            Err(_) => break,
+        }
+    }
+
+    assert!(
+        peer_change_count <= config.peerset_inbound_connection_limit(),
+        "unexpected number of peer changes {}, over limit of {}, had {} peer trackers",
+        peer_change_count,
+        config.peerset_inbound_connection_limit(),
+        peer_tracker_count,
+    );
+
+    assert!(
+        peer_tracker_count <= config.peerset_inbound_connection_limit(),
+        "unexpected number of peer trackers {}, over limit of {}, had {} peer changes",
+        peer_tracker_count,
+        config.peerset_inbound_connection_limit(),
+        peer_change_count,
     );
 }
 
@@ -801,6 +1334,102 @@ where
     (config, peerset_rx)
 }
 
+/// Run an inbound peer listener with `peerset_initial_target_size` and `handshaker`.
+///
+/// Uses the default values for all other config fields.
+///
+/// Returns the generated [`Config`], and the peer set receiver.
+async fn spawn_inbound_listener_with_peer_limit<S>(
+    peerset_initial_target_size: impl Into<Option<usize>>,
+    listen_handshaker: S,
+) -> (Config, mpsc::Receiver<PeerChange>)
+where
+    S: Service<peer::HandshakeRequest, Response = peer::Client, Error = BoxError>
+        + Clone
+        + Send
+        + 'static,
+    S::Future: Send + 'static,
+{
+    // Create a test config that listens on any unused port.
+    let listen_addr = "127.0.0.1:0".parse().unwrap();
+    let mut config = Config {
+        listen_addr,
+        ..Config::default()
+    };
+
+    if let Some(peerset_initial_target_size) = peerset_initial_target_size.into() {
+        config.peerset_initial_target_size = peerset_initial_target_size;
+    }
+
+    // Open the listener port.
+    let (tcp_listener, listen_addr) = open_listener(&config.clone()).await;
+
+    // Make enough inbound connections to go over the limit, even if the limit is zero.
+    // Make the channels large enough to hold all the connections.
+    let over_limit_connections = config.peerset_inbound_connection_limit() * 2 + 1;
+    let (peerset_tx, peerset_rx) = mpsc::channel::<PeerChange>(over_limit_connections);
+
+    // Start listening for connections.
+    let listen_fut = accept_inbound_connections(
+        config.clone(),
+        tcp_listener,
+        listen_handshaker,
+        peerset_tx.clone(),
+    );
+    let listen_task_handle = tokio::spawn(listen_fut);
+
+    // Open inbound connections.
+    let mut outbound_task_handles = Vec::new();
+    for _ in 0..over_limit_connections {
+        let outbound_fut = async move {
+            let outbound_result = TcpStream::connect(listen_addr).await;
+            // Let other tasks run before we block on reading.
+            tokio::task::yield_now().await;
+
+            if let Ok(outbound_stream) = outbound_result {
+                // Wait until the listener closes the connection.
+                // The handshaker is fake, so it never sends any data.
+                let readable_result = outbound_stream.readable().await;
+                info!(
+                    ?readable_result,
+                    "outbound connection became readable or errored: \
+                     closing connection to test inbound listener"
+                );
+            } else {
+                // If the connection is closed quickly, we might get errors here.
+                debug!(
+                    ?outbound_result,
+                    "outbound connection error in inbound listener test"
+                );
+            }
+        };
+
+        let outbound_task_handle = tokio::spawn(outbound_fut);
+        outbound_task_handles.push(outbound_task_handle);
+    }
+
+    // Let the listener run for a while.
+    tokio::time::sleep(LISTENER_TEST_DURATION).await;
+
+    // Stop the listener and outbound tasks, and let them finish.
+    listen_task_handle.abort();
+    for outbound_task_handle in outbound_task_handles {
+        outbound_task_handle.abort();
+    }
+    tokio::task::yield_now().await;
+
+    // Check for panics or errors in the listener.
+    let listen_result = listen_task_handle.now_or_never();
+    assert!(
+        matches!(listen_result, None)
+            || matches!(listen_result, Some(Err(ref e)) if e.is_cancelled()),
+        "unexpected error or panic in inbound peer listener task: {:?}",
+        listen_result,
+    );
+
+    (config, peerset_rx)
+}
+
 /// Initialize a task that connects to `peer_count` initial peers using the
 /// given connector.
 ///
diff --git a/zebra-network/src/peer_set/set.rs b/zebra-network/src/peer_set/set.rs
index d224d2568..653185996 100644
--- a/zebra-network/src/peer_set/set.rs
+++ b/zebra-network/src/peer_set/set.rs
@@ -80,7 +80,7 @@ use crate::{
         external::InventoryHash,
         internal::{Request, Response},
     },
-    AddressBook, BoxError,
+    AddressBook, BoxError, Config,
 };
 
 /// A signal sent by the [`PeerSet`] when it has no ready peers, and gets a request from Zebra.
@@ -134,6 +134,8 @@ where
     ///
     /// Used for logging diagnostics.
     address_book: Arc<std::sync::Mutex<AddressBook>>,
+    /// The configured limit for inbound and outbound connections.
+    peerset_total_connection_limit: usize,
 }
 
 impl<D> PeerSet<D>
@@ -147,6 +149,7 @@ where
 {
     /// Construct a peerset which uses `discover` internally.
     pub fn new(
+        config: &Config,
         discover: D,
         demand_signal: mpsc::Sender<MorePeers>,
         handle_rx: tokio::sync::oneshot::Receiver<Vec<JoinHandle<Result<(), BoxError>>>>,
@@ -165,6 +168,7 @@ where
             inventory_registry: InventoryRegistry::new(inv_stream),
             last_peer_log: None,
             address_book,
+            peerset_total_connection_limit: config.peerset_total_connection_limit(),
         }
     }
 
@@ -432,6 +436,17 @@ where
         metrics::gauge!("pool.num_ready", num_ready as f64);
         metrics::gauge!("pool.num_unready", num_unready as f64);
         metrics::gauge!("zcash.net.peers", num_peers as f64);
+
+        // Security: make sure we haven't exceeded the connection limit
+        if num_peers > self.peerset_total_connection_limit {
+            let address_metrics = self.address_book.lock().unwrap().address_metrics();
+            panic!(
+                "unexpectedly exceeded configured peer set connection limit: \n\
+                 peers: {:?}, ready: {:?}, unready: {:?}, \n\
+                 address_metrics: {:?}",
+                num_peers, num_ready, num_unready, address_metrics,
+            );
+        }
     }
 }