diff --git a/src/Avalonia.Controls/ApplicationLifetimes/ClassicDesktopStyleApplicationLifetime.cs b/src/Avalonia.Controls/ApplicationLifetimes/ClassicDesktopStyleApplicationLifetime.cs
index 2a42d99ac5..3a2fd68af5 100644
--- a/src/Avalonia.Controls/ApplicationLifetimes/ClassicDesktopStyleApplicationLifetime.cs
+++ b/src/Avalonia.Controls/ApplicationLifetimes/ClassicDesktopStyleApplicationLifetime.cs
@@ -2,6 +2,7 @@ using System;
 using System.Collections.Generic;
 using System.ComponentModel;
 using System.Linq;
+using System.Runtime.CompilerServices;
 using System.Threading;
 using Avalonia.Controls;
 using Avalonia.Controls.ApplicationLifetimes;
@@ -122,12 +123,23 @@ namespace Avalonia.Controls.ApplicationLifetimes
                 lifetimeEvents.ShutdownRequested += OnShutdownRequested;
 
             _cts = new CancellationTokenSource();
-            MainWindow?.Show();
+            
+            // Note due to a bug in the JIT we wrap this in a method, otherwise MainWindow
+            // gets stuffed into a local var and can not be GCed until after the program stops.
+            // this method never exits until program end.
+            ShowMainWindow(); 
+                              
             Dispatcher.UIThread.MainLoop(_cts.Token);
             Environment.ExitCode = _exitCode;
             return _exitCode;
         }
 
+        [MethodImpl(MethodImplOptions.NoInlining)]
+        private void ShowMainWindow()
+        {
+            MainWindow?.Show();
+        }
+
         public void Dispose()
         {
             if (_activeLifetime == this)
diff --git a/src/Avalonia.Controls/WindowBase.cs b/src/Avalonia.Controls/WindowBase.cs
index ee008efb04..5861d0452d 100644
--- a/src/Avalonia.Controls/WindowBase.cs
+++ b/src/Avalonia.Controls/WindowBase.cs
@@ -193,6 +193,12 @@ namespace Avalonia.Controls
             try
             {
                 IsVisible = false;
+                
+                if (this is IFocusScope scope)
+                {
+                    FocusManager.Instance?.RemoveFocusScope(scope);
+                }
+                
                 base.HandleClosed();
             }
             finally
diff --git a/src/Avalonia.Input/ApiCompatBaseline.txt b/src/Avalonia.Input/ApiCompatBaseline.txt
index 98eb8598d8..270c5305e5 100644
--- a/src/Avalonia.Input/ApiCompatBaseline.txt
+++ b/src/Avalonia.Input/ApiCompatBaseline.txt
@@ -3,6 +3,7 @@ MembersMustExist : Member 'public Avalonia.Platform.IPlatformHandle Avalonia.Inp
 MembersMustExist : Member 'public Avalonia.Interactivity.RoutedEvent<Avalonia.Interactivity.RoutedEventArgs> Avalonia.Interactivity.RoutedEvent<Avalonia.Interactivity.RoutedEventArgs> Avalonia.Input.Gestures.DoubleTappedEvent' does not exist in the implementation but it does exist in the contract.
 MembersMustExist : Member 'public Avalonia.Interactivity.RoutedEvent<Avalonia.Interactivity.RoutedEventArgs> Avalonia.Interactivity.RoutedEvent<Avalonia.Interactivity.RoutedEventArgs> Avalonia.Input.Gestures.RightTappedEvent' does not exist in the implementation but it does exist in the contract.
 MembersMustExist : Member 'public Avalonia.Interactivity.RoutedEvent<Avalonia.Interactivity.RoutedEventArgs> Avalonia.Interactivity.RoutedEvent<Avalonia.Interactivity.RoutedEventArgs> Avalonia.Input.Gestures.TappedEvent' does not exist in the implementation but it does exist in the contract.
+InterfacesShouldHaveSameMembers : Interface member 'public void Avalonia.Input.IFocusManager.RemoveFocusScope(Avalonia.Input.IFocusScope)' is present in the implementation but not in the contract.
 MembersMustExist : Member 'public Avalonia.Interactivity.RoutedEvent<Avalonia.Interactivity.RoutedEventArgs> Avalonia.Interactivity.RoutedEvent<Avalonia.Interactivity.RoutedEventArgs> Avalonia.Input.InputElement.DoubleTappedEvent' does not exist in the implementation but it does exist in the contract.
 MembersMustExist : Member 'public Avalonia.Interactivity.RoutedEvent<Avalonia.Interactivity.RoutedEventArgs> Avalonia.Interactivity.RoutedEvent<Avalonia.Interactivity.RoutedEventArgs> Avalonia.Input.InputElement.TappedEvent' does not exist in the implementation but it does exist in the contract.
 MembersMustExist : Member 'public void Avalonia.Input.InputElement.add_DoubleTapped(System.EventHandler<Avalonia.Interactivity.RoutedEventArgs>)' does not exist in the implementation but it does exist in the contract.
@@ -10,4 +11,4 @@ MembersMustExist : Member 'public void Avalonia.Input.InputElement.add_Tapped(Sy
 MembersMustExist : Member 'public void Avalonia.Input.InputElement.remove_DoubleTapped(System.EventHandler<Avalonia.Interactivity.RoutedEventArgs>)' does not exist in the implementation but it does exist in the contract.
 MembersMustExist : Member 'public void Avalonia.Input.InputElement.remove_Tapped(System.EventHandler<Avalonia.Interactivity.RoutedEventArgs>)' does not exist in the implementation but it does exist in the contract.
 TypesMustExist : Type 'Avalonia.Platform.IStandardCursorFactory' does not exist in the implementation but it does exist in the contract.
-Total Issues: 11
+Total Issues: 12
diff --git a/src/Avalonia.Input/FocusManager.cs b/src/Avalonia.Input/FocusManager.cs
index 1432092ba1..2efd33df1d 100644
--- a/src/Avalonia.Input/FocusManager.cs
+++ b/src/Avalonia.Input/FocusManager.cs
@@ -162,6 +162,22 @@ namespace Avalonia.Input
             Focus(e);
         }
 
+        public void RemoveFocusScope(IFocusScope scope)
+        {
+            scope = scope ?? throw new ArgumentNullException(nameof(scope));
+            
+            if (_focusScopes.TryGetValue(scope, out _))
+            {
+                SetFocusedElement(scope, null);
+                _focusScopes.Remove(scope);
+            }
+
+            if (Scope == scope)
+            {
+                Scope = null;
+            }
+        }
+
         public static bool GetIsFocusScope(IInputElement e) => e is IFocusScope;
 
         /// <summary>
diff --git a/src/Avalonia.Input/IFocusManager.cs b/src/Avalonia.Input/IFocusManager.cs
index e1b5087c3d..2510479a8e 100644
--- a/src/Avalonia.Input/IFocusManager.cs
+++ b/src/Avalonia.Input/IFocusManager.cs
@@ -35,5 +35,13 @@ namespace Avalonia.Input
         /// when it activates, e.g. when a Window is activated.
         /// </remarks>
         void SetFocusScope(IFocusScope scope);
+
+        /// <summary>
+        /// Notifies the focus manager that a focus scope has been removed.
+        /// </summary>
+        /// <param name="scope">The focus scope to be removed.</param>
+        /// This should not be called by client code. It is called by an <see cref="IFocusScope"/>
+        /// when it deactivates or closes, e.g. when a Window is closed.
+        void RemoveFocusScope(IFocusScope scope);
     }
 }