diff --git a/src/Avalonia.Controls/Control.cs b/src/Avalonia.Controls/Control.cs
index ebfe98a175..94ad985046 100644
--- a/src/Avalonia.Controls/Control.cs
+++ b/src/Avalonia.Controls/Control.cs
@@ -110,6 +110,11 @@ namespace Avalonia.Controls
         /// <inheritdoc/>
         void ISetterValue.Initialize(ISetter setter)
         {
+            if (setter is Setter s && s.Property == ContextFlyoutProperty)
+            {
+                return; // Allow ContextFlyout to not need wrapping in <Template>
+            }
+
             throw new InvalidOperationException(
                 "Cannot use a control as a Setter value. Wrap the control in a <Template>.");
         }
diff --git a/src/Avalonia.Controls/Flyouts/Flyout.cs b/src/Avalonia.Controls/Flyouts/Flyout.cs
index ff6f78a6f4..b1ca15bb4e 100644
--- a/src/Avalonia.Controls/Flyouts/Flyout.cs
+++ b/src/Avalonia.Controls/Flyouts/Flyout.cs
@@ -38,10 +38,11 @@ namespace Avalonia.Controls
         {
             if (FlyoutPresenterClasses != null)
             {
-                //Remove any classes no longer in use
+                //Remove any classes no longer in use, ignoring any pseudoclasses
                 for (int i = _popup.Child.Classes.Count - 1; i >= 0; i--)
                 {
-                    if (!FlyoutPresenterClasses.Contains(_popup.Child.Classes[i]))
+                    if (!FlyoutPresenterClasses.Contains(_popup.Child.Classes[i]) && 
+                        !_popup.Child.Classes[i].Contains(":"))
                     {
                         _popup.Child.Classes.RemoveAt(i);
                     }
diff --git a/src/Avalonia.Controls/Flyouts/MenuFlyout.cs b/src/Avalonia.Controls/Flyouts/MenuFlyout.cs
index 4cea5199f1..f147719281 100644
--- a/src/Avalonia.Controls/Flyouts/MenuFlyout.cs
+++ b/src/Avalonia.Controls/Flyouts/MenuFlyout.cs
@@ -58,10 +58,11 @@ namespace Avalonia.Controls
         {
             if (FlyoutPresenterClasses != null)
             {
-                //Remove any classes no longer in use
+                //Remove any classes no longer in use, ignoring pseudoclasses
                 for (int i = _popup.Child.Classes.Count - 1; i >= 0; i--)
                 {
-                    if (!FlyoutPresenterClasses.Contains(_popup.Child.Classes[i]))
+                    if (!FlyoutPresenterClasses.Contains(_popup.Child.Classes[i]) && 
+                        !_popup.Child.Classes[i].Contains(":"))
                     {
                         _popup.Child.Classes.RemoveAt(i);
                     }