diff --git a/Terminal.Gui/App/Application.Driver.cs b/Terminal.Gui/App/Application.Driver.cs
index aa2ee80fe..3671ee519 100644
--- a/Terminal.Gui/App/Application.Driver.cs
+++ b/Terminal.Gui/App/Application.Driver.cs
@@ -6,6 +6,12 @@ public static partial class Application // Driver abstractions
 {
     internal static bool _forceFakeConsole;
 
+    // Internal helper method for ApplicationImpl.ResetState to clear this field
+    internal static void ClearForceFakeConsole ()
+    {
+        _forceFakeConsole = false;
+    }
+
     /// <summary>Gets the <see cref="IConsoleDriver"/> that has been selected. See also <see cref="ForceDriver"/>.</summary>
     public static IConsoleDriver? Driver
     {
diff --git a/Terminal.Gui/App/Application.Run.cs b/Terminal.Gui/App/Application.Run.cs
index 2aba0f7e3..d6dbb6728 100644
--- a/Terminal.Gui/App/Application.Run.cs
+++ b/Terminal.Gui/App/Application.Run.cs
@@ -46,6 +46,7 @@ public static partial class Application // Run (Begin -> Run -> Layout/Draw -> E
     {
         NotifyNewRunState = null;
         NotifyStopRunState = null;
+        Iteration = null;
     }
 
     /// <summary>Building block API: Prepares the provided <see cref="Toplevel"/> for execution.</summary>
diff --git a/Terminal.Gui/App/ApplicationImpl.cs b/Terminal.Gui/App/ApplicationImpl.cs
index 007af49ae..decbfe5d8 100644
--- a/Terminal.Gui/App/ApplicationImpl.cs
+++ b/Terminal.Gui/App/ApplicationImpl.cs
@@ -633,6 +633,11 @@ public class ApplicationImpl : IApplication
         _cachedRunStateToplevel = null;
 
         _mainThreadId = -1;
+        
+        // These static properties need to be reset
+        Application.EndAfterFirstIteration = false;
+        Application.ClearScreenNextIteration = false;
+        Application.ClearForceFakeConsole ();
 
         // Driver stuff
         if (_driver is { })
@@ -664,6 +669,9 @@ public class ApplicationImpl : IApplication
 
         _navigation = null;
 
+        // Reset SupportedCultures so it's re-cached on next access
+        _supportedCultures = null;
+
         // Reset synchronization context to allow the user to run async/await,
         // as the main loop has been ended, the synchronization context from
         // gui.cs does no longer process any callbacks. See #1084 for more details: