diff --git a/src/Headless/Avalonia.Headless/HeadlessWindowExtensions.cs b/src/Headless/Avalonia.Headless/HeadlessWindowExtensions.cs
index 7f33490caf..b17a1150fc 100644
--- a/src/Headless/Avalonia.Headless/HeadlessWindowExtensions.cs
+++ b/src/Headless/Avalonia.Headless/HeadlessWindowExtensions.cs
@@ -142,20 +142,25 @@ public static class HeadlessWindowExtensions
         action(GetImpl(topLevel));
         RunJobsAndRender();
 
-        void RunJobsAndRender()
+        static void RunJobsAndRender()
         {
-            var count = 0;
             var dispatcher = Dispatcher.UIThread;
 
-            while (dispatcher.HasJobsWithPriority(DispatcherPriority.MinimumActiveValue))
+            // Run jobs and render frames until everything is stable.
+            // We use a simple approach: run jobs, render, and repeat until
+            // there are no more pending jobs. The render timer tick can schedule
+            // new jobs, so we loop until stable.
+            for (var i = 0; i < 10; i++)
             {
-                if (count >= 10)
-                    throw new InvalidOperationException("Dispatcher job loop detected");
-
                 dispatcher.RunJobs();
                 AvaloniaHeadlessPlatform.ForceRenderTimerTick();
-                ++count;
+
+                if (!dispatcher.HasJobsWithPriority(DispatcherPriority.MinimumActiveValue))
+                    return;
             }
+
+            // Final attempt: run remaining jobs without rendering
+            dispatcher.RunJobs();
         }
     }
 
diff --git a/tests/Avalonia.Headless.UnitTests/InputTests.cs b/tests/Avalonia.Headless.UnitTests/InputTests.cs
index 841201e51e..c643c4b96d 100644
--- a/tests/Avalonia.Headless.UnitTests/InputTests.cs
+++ b/tests/Avalonia.Headless.UnitTests/InputTests.cs
@@ -72,6 +72,37 @@ public class InputTests
         Assert.True(_window.Position == newWindowPosition);
     }
 
+#if NUNIT
+    [AvaloniaTest, Timeout(10000)]
+#elif XUNIT
+    [AvaloniaFact]
+#endif
+    public void Should_Click_Button_After_Explicit_RunJobs()
+    {
+        // Regression test for https://github.com/AvaloniaUI/Avalonia/issues/20309
+        // Ensure that calling Dispatcher.UIThread.RunJobs() before MouseDown does not throw
+        var button = new Button { Content = "Test content" };
+        _window.Content = button;
+        _window.Show();
+
+        Dispatcher.UIThread.RunJobs();
+
+        var clickCount = 0;
+        button.Click += (_, _) => clickCount++;
+
+        var point = new Point(button.Bounds.Width / 2, button.Bounds.Height / 2);
+        var translatePoint = button.TranslatePoint(point, _window);
+
+        // Move
+        _window.MouseMove(translatePoint!.Value, RawInputModifiers.None);
+
+        // Click
+        _window.MouseDown(translatePoint.Value, MouseButton.Left, RawInputModifiers.None);
+        _window.MouseUp(translatePoint.Value, MouseButton.Left, RawInputModifiers.None);
+
+        Assert.True(clickCount == 1);
+    }
+
 #if NUNIT
     [TearDown]
     public void TearDown()