diff --git a/agent/agent_test.go b/agent/agent_test.go
index 31f1448f34018..6cef939d47a4c 100644
--- a/agent/agent_test.go
+++ b/agent/agent_test.go
@@ -1547,32 +1547,33 @@ func TestAgent_Dial(t *testing.T) {
 		t.Run(c.name, func(t *testing.T) {
 			t.Parallel()
 
-			// Setup listener
+			// The purpose of this test is to ensure that a client can dial a
+			// listener in the workspace over tailnet.
 			l := c.setup(t)
-			defer l.Close()
-			go func() {
-				for {
-					c, err := l.Accept()
-					if err != nil {
-						return
-					}
+			done := make(chan struct{})
+			defer func() {
+				l.Close()
+				<-done
+			}()
 
-					go testAccept(t, c)
-				}
+			ctx, cancel := context.WithTimeout(context.Background(), testutil.WaitLong)
+			defer cancel()
+
+			go func() {
+				defer close(done)
+				c, err := l.Accept()
+				assert.NoError(t, err, "accept connection")
+				defer c.Close()
+				testAccept(ctx, t, c)
 			}()
 
 			//nolint:dogsled
-			conn, _, _, _, _ := setupAgent(t, agentsdk.Manifest{}, 0)
-			require.True(t, conn.AwaitReachable(context.Background()))
-			conn1, err := conn.DialContext(context.Background(), l.Addr().Network(), l.Addr().String())
+			agentConn, _, _, _, _ := setupAgent(t, agentsdk.Manifest{}, 0)
+			require.True(t, agentConn.AwaitReachable(ctx))
+			conn, err := agentConn.DialContext(ctx, l.Addr().Network(), l.Addr().String())
 			require.NoError(t, err)
-			defer conn1.Close()
-			conn2, err := conn.DialContext(context.Background(), l.Addr().Network(), l.Addr().String())
-			require.NoError(t, err)
-			defer conn2.Close()
-			testDial(t, conn2)
-			testDial(t, conn1)
-			time.Sleep(150 * time.Millisecond)
+			defer conn.Close()
+			testDial(ctx, t, conn)
 		})
 	}
 }
@@ -2002,22 +2003,41 @@ func setupAgent(t *testing.T, metadata agentsdk.Manifest, ptyTimeout time.Durati
 
 var dialTestPayload = []byte("dean-was-here123")
 
-func testDial(t *testing.T, c net.Conn) {
+func testDial(ctx context.Context, t *testing.T, c net.Conn) {
 	t.Helper()
 
+	if deadline, ok := ctx.Deadline(); ok {
+		err := c.SetDeadline(deadline)
+		assert.NoError(t, err)
+		defer func() {
+			err := c.SetDeadline(time.Time{})
+			assert.NoError(t, err)
+		}()
+	}
+
 	assertWritePayload(t, c, dialTestPayload)
 	assertReadPayload(t, c, dialTestPayload)
 }
 
-func testAccept(t *testing.T, c net.Conn) {
+func testAccept(ctx context.Context, t *testing.T, c net.Conn) {
 	t.Helper()
 	defer c.Close()
 
+	if deadline, ok := ctx.Deadline(); ok {
+		err := c.SetDeadline(deadline)
+		assert.NoError(t, err)
+		defer func() {
+			err := c.SetDeadline(time.Time{})
+			assert.NoError(t, err)
+		}()
+	}
+
 	assertReadPayload(t, c, dialTestPayload)
 	assertWritePayload(t, c, dialTestPayload)
 }
 
 func assertReadPayload(t *testing.T, r io.Reader, payload []byte) {
+	t.Helper()
 	b := make([]byte, len(payload)+16)
 	n, err := r.Read(b)
 	assert.NoError(t, err, "read payload")
@@ -2026,6 +2046,7 @@ func assertReadPayload(t *testing.T, r io.Reader, payload []byte) {
 }
 
 func assertWritePayload(t *testing.T, w io.Writer, payload []byte) {
+	t.Helper()
 	n, err := w.Write(payload)
 	assert.NoError(t, err, "write payload")
 	assert.Equal(t, len(payload), n, "payload length does not match")