diff --git a/pkg/ssh/forward.go b/pkg/ssh/forward.go
index f273e20e2..f87d3ce10 100644
--- a/pkg/ssh/forward.go
+++ b/pkg/ssh/forward.go
@@ -18,6 +18,8 @@ import (
 // should check for this error with errors.Is.
 var ErrIdleTimeout = errors.New("port forward idle timeout")
 
+var ErrTransportClosed = errors.New("ssh transport closed")
+
 type ForwardingFunction func(
 	net.Conn,
 	*ssh.Client,
@@ -114,6 +116,23 @@ func portForwarding(
 		}
 	}()
 
+	if client != nil {
+		transportClosed := make(chan struct{})
+		go func() {
+			if werr := client.Wait(); werr != nil {
+				log.Debugf("ssh transport closed on %s: %v", srcAddr, werr)
+			}
+			close(transportClosed)
+		}()
+		go func() {
+			select {
+			case <-done:
+			case <-transportClosed:
+				cancel(ErrTransportClosed)
+			}
+		}()
+	}
+
 	counter := newConnectionCounter(fwdCtx, exitAfterTimeout, func() {
 		log.Infof(
 			"Stopping port-forward on %s: idle for a while. "+
@@ -126,10 +145,11 @@ func portForwarding(
 		// waiting for a new connection
 		connection, err := listener.Accept()
 		if err != nil {
-			// If shutdown was caused by the idle timeout, surface that
-			// typed error so callers can choose to treat it as a clean exit.
-			if cause := context.Cause(fwdCtx); errors.Is(cause, ErrIdleTimeout) {
+			switch cause := context.Cause(fwdCtx); {
+			case errors.Is(cause, ErrIdleTimeout):
 				return ErrIdleTimeout
+			case errors.Is(cause, ErrTransportClosed):
+				return ErrTransportClosed
 			}
 			return err
 		}
diff --git a/pkg/ssh/forward_test.go b/pkg/ssh/forward_test.go
index 6411f36d7..78152de83 100644
--- a/pkg/ssh/forward_test.go
+++ b/pkg/ssh/forward_test.go
@@ -2,6 +2,7 @@ package ssh
 
 import (
 	"context"
+	"crypto/ed25519"
 	"errors"
 	"net"
 	"testing"
@@ -91,3 +92,95 @@ func TestPortForwarding_ParentCancelNotIdleTimeout(t *testing.T) {
 		t.Fatal("timed out waiting for portForwarding to return")
 	}
 }
+
+func startTestSSHServer(t *testing.T) (client *ssh.Client, kill func()) {
+	t.Helper()
+
+	_, priv, err := ed25519.GenerateKey(nil)
+	if err != nil {
+		t.Fatalf("generate host key: %v", err)
+	}
+	signer, err := ssh.NewSignerFromKey(priv)
+	if err != nil {
+		t.Fatalf("signer: %v", err)
+	}
+
+	srvCfg := &ssh.ServerConfig{NoClientAuth: true}
+	srvCfg.AddHostKey(signer)
+
+	ln, err := net.Listen("tcp", "127.0.0.1:0")
+	if err != nil {
+		t.Fatalf("listen: %v", err)
+	}
+	t.Cleanup(func() { _ = ln.Close() })
+
+	serverConnCh := make(chan net.Conn, 1)
+	go func() {
+		nConn, aerr := ln.Accept()
+		if aerr != nil {
+			return
+		}
+		serverConnCh <- nConn
+		sConn, chans, reqs, herr := ssh.NewServerConn(nConn, srvCfg)
+		if herr != nil {
+			return
+		}
+		go ssh.DiscardRequests(reqs)
+		go func() {
+			for nc := range chans {
+				_ = nc.Reject(ssh.Prohibited, "no channels in test")
+			}
+		}()
+		_ = sConn
+	}()
+
+	cConn, err := ssh.Dial("tcp", ln.Addr().String(), &ssh.ClientConfig{
+		User:            "test",
+		HostKeyCallback: ssh.FixedHostKey(signer.PublicKey()),
+		Timeout:         2 * time.Second,
+	})
+	if err != nil {
+		t.Fatalf("dial: %v", err)
+	}
+
+	serverConn := <-serverConnCh
+	kill = func() {
+		_ = serverConn.Close()
+		_ = ln.Close()
+	}
+	t.Cleanup(func() { _ = cConn.Close(); kill() })
+	return cConn, kill
+}
+
+func TestPortForwarding_ReleasesListenerOnTransportDeath(t *testing.T) {
+	client, kill := startTestSSHServer(t)
+
+	lis, err := net.Listen("tcp", "127.0.0.1:0")
+	if err != nil {
+		t.Fatalf("listen: %v", err)
+	}
+	addr := lis.Addr().String()
+
+	done := make(chan error, 1)
+	go func() {
+		done <- portForwarding(t.Context(), client, lis, addr, "tcp", "127.0.0.1:9", 0, forward)
+	}()
+
+	time.Sleep(100 * time.Millisecond)
+	kill()
+
+	select {
+	case err := <-done:
+		if !errors.Is(err, ErrTransportClosed) {
+			t.Fatalf("expected ErrTransportClosed, got %v", err)
+		}
+	case <-time.After(3 * time.Second):
+		t.Fatal("portForwarding did not return after transport death (listener leaked)")
+	}
+
+	l2, err := net.Listen("tcp", addr)
+	if err != nil {
+		t.Fatalf("rebind on %s failed after transport death: %v", addr, err)
+	}
+	_ = l2.Close()
+}