diff --git a/integration/integration_test.go b/integration/integration_test.go
index 9084d9f64b233..b44ad9d3b0a5a 100644
--- a/integration/integration_test.go
+++ b/integration/integration_test.go
@@ -7557,13 +7557,40 @@ func testAgentlessConnection(t *testing.T, suite *integrationTestSuite) {
 		// so closing it here will result in io.EOF if the test passes
 		_ = session.Close()
 	})
-	require.NoError(t, agent.ForwardToAgent(sshClient, tc.LocalAgent()))
+
+	// this is essentially what agent.ForwardToAgent does, but we're
+	// doing it manually so can take ownership of the opened SSH channel
+	// and check that it's closed correctly
+	channels := sshClient.HandleChannelOpen("auth-agent@openssh.com")
+	require.NotNil(t, channels)
+
+	doneServing := make(chan error)
+	go func() {
+		for ch := range channels {
+			channel, reqs, err := ch.Accept()
+			assert.NoError(t, err)
+			go ssh.DiscardRequests(reqs)
+			go func() {
+				doneServing <- agent.ServeAgent(tc.LocalAgent(), channel)
+				channel.Close()
+			}()
+		}
+	}()
+
 	require.NoError(t, agent.RequestAgentForwarding(session))
 
 	// run a command
 	err = session.Run("cmd")
 	require.NoError(t, err)
 
+	// test that SSH agent channel is closed properly
+	select {
+	case err := <-doneServing:
+		require.ErrorIs(t, err, io.EOF)
+	case <-time.After(3 * time.Second):
+		require.Fail(t, "timeout waiting for SSH agent channel to be closed")
+	}
+
 	require.NoError(t, nodeClient.Close())
 }
 
diff --git a/lib/srv/forward/sshserver.go b/lib/srv/forward/sshserver.go
index cd8e21fdbae9b..bf0ec659c1d73 100644
--- a/lib/srv/forward/sshserver.go
+++ b/lib/srv/forward/sshserver.go
@@ -1161,6 +1161,7 @@ func (s *Server) handleAgentForward(ch ssh.Channel, req *ssh.Request, ctx *srv.S
 		if err != nil {
 			return trace.Wrap(err)
 		}
+		ctx.AddCloser(userAgent)
 	}
 
 	err = agent.ForwardToAgent(ctx.RemoteClient.Client, userAgent)