diff --git a/ILSpy.Tests/ContextMenus/DecompileInNewViewTests.cs b/ILSpy.Tests/ContextMenus/DecompileInNewViewTests.cs
index 0607a7527c..d1ca446d8f 100644
--- a/ILSpy.Tests/ContextMenus/DecompileInNewViewTests.cs
+++ b/ILSpy.Tests/ContextMenus/DecompileInNewViewTests.cs
@@ -250,6 +250,8 @@ ICSharpCode.ILSpy.Controls.TreeView.SharpTreeViewItem Row(SharpTreeNode node) =>
 			.OfType<ICSharpCode.ILSpy.Controls.TreeView.SharpTreeViewItem>()
 			.First(r => RowNodeEquals(r, node));
 
+		var menu = grid.ContextMenu!;
+
 		async Task RightClick(SharpTreeNode node)
 		{
 			var row = Row(node);
@@ -257,21 +259,23 @@ async Task RightClick(SharpTreeNode node)
 			var pt = row.TranslatePoint(new Point(clickX, row.Bounds.Height / 2), window);
 			HeadlessWindowExtensions.MouseDown(window, pt!.Value, MouseButton.Right);
 			HeadlessWindowExtensions.MouseUp(window, pt.Value, MouseButton.Right);
-			for (int i = 0; i < 4; i++)
-			{
-				Dispatcher.UIThread.RunJobs();
-				await Task.Delay(20);
-			}
+			// The highlight is scoped to the popup - set while the menu is being requested, dropped
+			// again when it closes - so the popup is the point at which the gesture is finished and
+			// the row's classes are worth reading.
+			await Waiters.WaitForAsync(() => menu.IsOpen, description: "the right-clicked row's context menu to open");
 		}
 
 		async Task Dismiss()
 		{
 			window.KeyPress(Key.Escape, RawInputModifiers.None, PhysicalKey.Escape, keySymbol: null);
+			await Waiters.WaitForAsync(() => !menu.IsOpen, description: "the context menu to close");
+			// IsOpen flips the moment the popup is torn down, but the frame that still shows its
+			// light-dismiss overlay is what answers hit tests until the scene is rendered again.
+			// Right-clicking into that frame delivers press and release to the vanishing overlay
+			// instead of the row: no ContextRequested is raised at all, so nothing becomes the
+			// context target and the next assertion sees a row with no classes on it.
 			for (int i = 0; i < 4; i++)
-			{
-				Dispatcher.UIThread.RunJobs();
-				await Task.Delay(20);
-			}
+				Waiters.PumpUI();
 		}
 
 		await RightClick(nodeB);
diff --git a/ILSpy.Tests/Waiters.cs b/ILSpy.Tests/Waiters.cs
index aaa63b1b5f..7b4393b000 100644
--- a/ILSpy.Tests/Waiters.cs
+++ b/ILSpy.Tests/Waiters.cs
@@ -22,6 +22,7 @@
 using System.Threading.Tasks;
 
 using Avalonia;
+using Avalonia.Headless;
 using Avalonia.Threading;
 using Avalonia.VisualTree;
 
@@ -51,13 +52,29 @@ public static async Task WaitForAsync(
 		{
 			if (predicate())
 				return;
-			Dispatcher.UIThread.RunJobs();
+			PumpUI();
 			await Task.Delay(PollInterval);
 		}
 		throw new TimeoutException(
 			$"Timed out after {(timeout ?? DefaultTimeout).TotalSeconds:0.#}s waiting for: {description}");
 	}
 
+	/// <summary>
+	/// Advances the UI by one step: runs the queued dispatcher jobs and renders a frame.
+	/// </summary>
+	/// <remarks>
+	/// Both halves matter. Hit testing for synthesized input is answered from the rendered scene,
+	/// not from the visual tree, so a loop that only runs dispatcher jobs leaves input routing a
+	/// frame behind: a click can still be delivered to a control the last frame shows but the tree
+	/// no longer has - a closed popup's light-dismiss overlay, for one - and never reach what is
+	/// underneath. Avalonia's own headless input helpers pump both for exactly this reason.
+	/// </remarks>
+	public static void PumpUI()
+	{
+		Dispatcher.UIThread.RunJobs();
+		AvaloniaHeadlessPlatform.ForceRenderTimerTick();
+	}
+
 	public static async Task WaitForAssembliesAsync(
 		this AssemblyTreeModel atm,
 		int minimumCount = 1,