diff --git a/src/Controls/src/Core/HandlerImpl/Application/Application.Impl.cs b/src/Controls/src/Core/HandlerImpl/Application/Application.Impl.cs
index f7edda731a9d..cc623971d061 100644
--- a/src/Controls/src/Core/HandlerImpl/Application/Application.Impl.cs
+++ b/src/Controls/src/Core/HandlerImpl/Application/Application.Impl.cs
@@ -1,5 +1,6 @@
 using System;
 using System.Collections.Generic;
+using System.Runtime.CompilerServices;
 using Microsoft.Extensions.Logging;
 using Microsoft.Maui.ApplicationModel;
 using Microsoft.Maui.Devices;
@@ -9,10 +10,10 @@ namespace Microsoft.Maui.Controls
 {
 	public partial class Application : IApplication
 	{
-		const string MauiWindowIdKey = "__MAUI_WINDOW_ID__";
+		internal const string MauiWindowIdKey = "__MAUI_WINDOW_ID__";
 
 		readonly List<Window> _windows = new();
-		readonly Dictionary<string, Window> _requestedWindows = new();
+		readonly Dictionary<string, WeakReference<Window>> _requestedWindows = new();
 		ILogger<Application>? _logger;
 
 		ILogger<Application>? Logger =>
@@ -29,8 +30,14 @@ IWindow IApplication.CreateWindow(IActivationState? activationState)
 			// try get the window that is pending
 			if (activationState?.State?.TryGetValue(MauiWindowIdKey, out var requestedWindowId) ?? false)
 			{
-				if (requestedWindowId != null && _requestedWindows.TryGetValue(requestedWindowId, out var w))
-					window = w;
+				if (requestedWindowId != null && _requestedWindows.TryGetValue(requestedWindowId, out var r))
+				{
+					if (r.TryGetTarget(out var w))
+					{
+						window = w;
+					}
+					_requestedWindows.Remove(requestedWindowId);
+				}
 			}
 
 			// create a new one if there is no pending windows
@@ -86,9 +93,8 @@ internal void RemoveWindow(Window window)
 
 		public virtual void OpenWindow(Window window)
 		{
-			var id = Guid.NewGuid().ToString();
-
-			_requestedWindows[id] = window;
+			var id = Guid.NewGuid().ToString("n");
+			_requestedWindows.Add(id, new WeakReference<Window>(window));
 
 			var state = new PersistedState
 			{
diff --git a/src/Controls/src/Core/HandlerImpl/Window/Window.Impl.cs b/src/Controls/src/Core/HandlerImpl/Window/Window.Impl.cs
index dd6fcb365d55..eb0e28e5a2d5 100644
--- a/src/Controls/src/Core/HandlerImpl/Window/Window.Impl.cs
+++ b/src/Controls/src/Core/HandlerImpl/Window/Window.Impl.cs
@@ -504,6 +504,7 @@ void IWindow.Destroying()
 			OnDestroying();
 
 			Application?.RemoveWindow(this);
+			Handler?.DisconnectHandler();
 		}
 
 		void IWindow.Resumed()
diff --git a/src/Controls/tests/Core.UnitTests/WindowsTests.cs b/src/Controls/tests/Core.UnitTests/WindowsTests.cs
index 6b063e341ae2..5ad99f8da81c 100644
--- a/src/Controls/tests/Core.UnitTests/WindowsTests.cs
+++ b/src/Controls/tests/Core.UnitTests/WindowsTests.cs
@@ -1,5 +1,8 @@
-using System.Collections.Generic;
+using System;
+using System.Collections;
+using System.Collections.Generic;
 using System.Linq;
+using System.Reflection;
 using System.Threading.Tasks;
 using Microsoft.Maui.Graphics;
 using Xunit;
@@ -621,5 +624,63 @@ public void MinDimensionsArePassedToCoreCorrectly(double inW, double inH, double
 			Assert.Equal(outW, coreWindow.MinimumWidth);
 			Assert.Equal(outH, coreWindow.MinimumHeight);
 		}
+
+		[Fact]
+		public async Task WindowDoesNotLeak()
+		{
+			var application = new Application();
+			WeakReference reference;
+
+			// Scope for window
+			{
+				var window = new Window { Page = new ContentPage() };
+				reference = new WeakReference(window);
+				application.OpenWindow(window);
+				((IWindow)window).Destroying();
+			}
+
+			// GC
+			await Task.Yield();
+			GC.Collect();
+			GC.WaitForPendingFinalizers();
+
+			Assert.False(reference.IsAlive, "Window should not be alive!");
+		}
+
+		// NOTE: this test is here to show `ConditionalWeakTable _requestedWindows` was a bad idea
+		[Fact]
+		public async Task TwoKeysSameWindow()
+		{
+			var application = new Application();
+			var window = new Window { Page = new ContentPage() };
+
+			application.OpenWindow(window);
+
+			// Access Application._requestedWindows
+			var flags = BindingFlags.NonPublic | BindingFlags.Instance;
+			var table = typeof(Application).GetField("_requestedWindows", flags).GetValue(application) as IDictionary;
+			Assert.NotNull(table);
+
+			// A "cloned" key should still work
+			string key;
+			{
+				var originalKey = table.Keys.OfType<string>().Single();
+				key = new string(originalKey);
+				Assert.NotSame(originalKey, key);
+			}
+
+			// GC collect the original key
+			await Task.Yield();
+			GC.Collect();
+			GC.WaitForPendingFinalizers();
+
+			// Same window, doesn't create a new one
+			var actual = ((IApplication)application).CreateWindow(new ActivationState(new MockMauiContext(), new PersistedState
+			{
+				{ Application.MauiWindowIdKey, key }
+			}));
+			Assert.Same(window, actual);
+			Assert.Empty(table);
+		}
 	}
 }