diff --git a/api/Avalonia.nupkg.xml b/api/Avalonia.nupkg.xml
index 1ff3e2fd3b..96f0ab5a30 100644
--- a/api/Avalonia.nupkg.xml
+++ b/api/Avalonia.nupkg.xml
@@ -301,6 +301,12 @@
     <Left>baseline/Avalonia/lib/net10.0/Avalonia.Controls.dll</Left>
     <Right>current/Avalonia/lib/net10.0/Avalonia.Controls.dll</Right>
   </Suppression>
+  <Suppression>
+    <DiagnosticId>CP0001</DiagnosticId>
+    <Target>T:Avalonia.Controls.Primitives.ChromeOverlayLayer</Target>
+    <Left>baseline/Avalonia/lib/net10.0/Avalonia.Controls.dll</Left>
+    <Right>current/Avalonia/lib/net10.0/Avalonia.Controls.dll</Right>
+  </Suppression>
   <Suppression>
     <DiagnosticId>CP0001</DiagnosticId>
     <Target>T:Avalonia.Controls.Primitives.IPopupHost</Target>
@@ -667,6 +673,12 @@
     <Left>baseline/Avalonia/lib/net8.0/Avalonia.Controls.dll</Left>
     <Right>current/Avalonia/lib/net8.0/Avalonia.Controls.dll</Right>
   </Suppression>
+  <Suppression>
+    <DiagnosticId>CP0001</DiagnosticId>
+    <Target>T:Avalonia.Controls.Primitives.ChromeOverlayLayer</Target>
+    <Left>baseline/Avalonia/lib/net8.0/Avalonia.Controls.dll</Left>
+    <Right>current/Avalonia/lib/net8.0/Avalonia.Controls.dll</Right>
+  </Suppression>
   <Suppression>
     <DiagnosticId>CP0001</DiagnosticId>
     <Target>T:Avalonia.Controls.Primitives.IPopupHost</Target>
@@ -1291,6 +1303,12 @@
     <Left>baseline/Avalonia/lib/net10.0/Avalonia.Controls.dll</Left>
     <Right>current/Avalonia/lib/net10.0/Avalonia.Controls.dll</Right>
   </Suppression>
+  <Suppression>
+    <DiagnosticId>CP0002</DiagnosticId>
+    <Target>F:Avalonia.Controls.Primitives.VisualLayerManager.ChromeOverlayLayerProperty</Target>
+    <Left>baseline/Avalonia/lib/net10.0/Avalonia.Controls.dll</Left>
+    <Right>current/Avalonia/lib/net10.0/Avalonia.Controls.dll</Right>
+  </Suppression>
   <Suppression>
     <DiagnosticId>CP0002</DiagnosticId>
     <Target>F:Avalonia.Controls.TextBlock.LetterSpacingProperty</Target>
@@ -1615,6 +1633,12 @@
     <Left>baseline/Avalonia/lib/net10.0/Avalonia.Controls.dll</Left>
     <Right>current/Avalonia/lib/net10.0/Avalonia.Controls.dll</Right>
   </Suppression>
+  <Suppression>
+    <DiagnosticId>CP0002</DiagnosticId>
+    <Target>M:Avalonia.Controls.Primitives.VisualLayerManager.get_ChromeOverlayLayer</Target>
+    <Left>baseline/Avalonia/lib/net10.0/Avalonia.Controls.dll</Left>
+    <Right>current/Avalonia/lib/net10.0/Avalonia.Controls.dll</Right>
+  </Suppression>
   <Suppression>
     <DiagnosticId>CP0002</DiagnosticId>
     <Target>M:Avalonia.Controls.Primitives.VisualLayerManager.get_LightDismissOverlayLayer</Target>
@@ -2377,6 +2401,12 @@
     <Left>baseline/Avalonia/lib/net8.0/Avalonia.Controls.dll</Left>
     <Right>current/Avalonia/lib/net8.0/Avalonia.Controls.dll</Right>
   </Suppression>
+  <Suppression>
+    <DiagnosticId>CP0002</DiagnosticId>
+    <Target>F:Avalonia.Controls.Primitives.VisualLayerManager.ChromeOverlayLayerProperty</Target>
+    <Left>baseline/Avalonia/lib/net8.0/Avalonia.Controls.dll</Left>
+    <Right>current/Avalonia/lib/net8.0/Avalonia.Controls.dll</Right>
+  </Suppression>
   <Suppression>
     <DiagnosticId>CP0002</DiagnosticId>
     <Target>F:Avalonia.Controls.TextBlock.LetterSpacingProperty</Target>
@@ -2701,6 +2731,12 @@
     <Left>baseline/Avalonia/lib/net8.0/Avalonia.Controls.dll</Left>
     <Right>current/Avalonia/lib/net8.0/Avalonia.Controls.dll</Right>
   </Suppression>
+  <Suppression>
+    <DiagnosticId>CP0002</DiagnosticId>
+    <Target>M:Avalonia.Controls.Primitives.VisualLayerManager.get_ChromeOverlayLayer</Target>
+    <Left>baseline/Avalonia/lib/net8.0/Avalonia.Controls.dll</Left>
+    <Right>current/Avalonia/lib/net8.0/Avalonia.Controls.dll</Right>
+  </Suppression>
   <Suppression>
     <DiagnosticId>CP0002</DiagnosticId>
     <Target>M:Avalonia.Controls.Primitives.VisualLayerManager.get_LightDismissOverlayLayer</Target>
diff --git a/src/Avalonia.Controls/Primitives/ChromeOverlayLayer.cs b/src/Avalonia.Controls/Primitives/ChromeOverlayLayer.cs
index 74b5beecad..d925a7a70c 100644
--- a/src/Avalonia.Controls/Primitives/ChromeOverlayLayer.cs
+++ b/src/Avalonia.Controls/Primitives/ChromeOverlayLayer.cs
@@ -4,27 +4,8 @@ using Avalonia.VisualTree;
 
 namespace Avalonia.Controls.Primitives
 {
-    public class ChromeOverlayLayer : Panel
+    internal class ChromeOverlayLayer : Panel
     {
-        public static Panel? GetOverlayLayer(Visual visual)
-        {
-            foreach (var v in visual.GetVisualAncestors())
-                if (v is VisualLayerManager vlm)
-                    if (vlm.OverlayLayer != null)
-                        return vlm.ChromeOverlayLayer;
 
-            if (visual is TopLevel tl)
-            {
-                var layers = tl.GetVisualDescendants().OfType<VisualLayerManager>().FirstOrDefault();
-                return layers?.ChromeOverlayLayer;
-            }
-
-            return null;
-        }
-
-        public void Add(Control c)
-        {
-            base.Children.Add(c);
-        }
     }
 }
diff --git a/src/Avalonia.Controls/Primitives/VisualLayerManager.cs b/src/Avalonia.Controls/Primitives/VisualLayerManager.cs
index 4c4f4f6b44..18a50fb5c0 100644
--- a/src/Avalonia.Controls/Primitives/VisualLayerManager.cs
+++ b/src/Avalonia.Controls/Primitives/VisualLayerManager.cs
@@ -1,4 +1,5 @@
 using System.Collections.Generic;
+using Avalonia.Controls.Chrome;
 using Avalonia.LogicalTree;
 
 namespace Avalonia.Controls.Primitives
@@ -14,9 +15,6 @@ namespace Avalonia.Controls.Primitives
         private ILogicalRoot? _logicalRoot;
         private readonly List<Control> _layers = new();
 
-        public static readonly StyledProperty<ChromeOverlayLayer?> ChromeOverlayLayerProperty =
-            AvaloniaProperty.Register<VisualLayerManager, ChromeOverlayLayer?>(nameof(ChromeOverlayLayer));
-
         public bool IsPopup { get; set; }
 
         internal AdornerLayer AdornerLayer
@@ -30,29 +28,42 @@ namespace Avalonia.Controls.Primitives
             }
         }
 
-        [System.Diagnostics.CodeAnalysis.SuppressMessage("AvaloniaProperty", "AVP1030")]
-        [System.Diagnostics.CodeAnalysis.SuppressMessage("AvaloniaProperty", "AVP1031",
-            Justification = "A hack to make ChromeOverlayLayer lazily creatable. It is expected that GetValue(ChromeOverlayLayerProperty) alone won't work.")]
-        public ChromeOverlayLayer ChromeOverlayLayer
-        {
-            get
-            {
-                var current = GetValue(ChromeOverlayLayerProperty);
 
-                if (current is null)
-                {
-                    var chromeOverlayLayer = new ChromeOverlayLayer();
-                    AddLayer(chromeOverlayLayer, ChromeZIndex);
+        protected override void OnAttachedToVisualTree(VisualTreeAttachmentEventArgs e)
+        {
+            EnsureChromeOverlayIfNeeded();
+            
+            base.OnAttachedToVisualTree(e);
+        }
 
-                    SetValue(ChromeOverlayLayerProperty, chromeOverlayLayer);
+        void EnsureChromeOverlayIfNeeded()
+        {
+            // HACK: This is a replacement hack for the old set of hacks for TitleBar.
 
-                    current = chromeOverlayLayer;
+            // Check if we are attached direclty-ish to a Window (i. e. no other VisualLayerManager in between).
+            // If we are, then we are the "main" VisualLayerManager and should create the ChromeOverlayLayer and add titlebar there
+            var parent = VisualParent;
+            while (parent != null)
+            {
+                if(parent is VisualLayerManager)
+                    break;
+                else if (parent is Window window)
+                {
+                    if (FindLayer<ChromeOverlayLayer>() == null)
+                    {
+                        var layer = new ChromeOverlayLayer();
+                        AddLayer(layer, ChromeZIndex);
+                        layer.Children.Add(new TitleBar());
+                    }
+                    
+                    break;
                 }
 
-                return current;
+                parent = parent.VisualParent;
+
             }
         }
-
+        
         internal OverlayLayer? OverlayLayer
         {
             get
diff --git a/src/Avalonia.Themes.Fluent/Controls/Window.xaml b/src/Avalonia.Themes.Fluent/Controls/Window.xaml
index 52d16e7ada..f56c9fbd10 100644
--- a/src/Avalonia.Themes.Fluent/Controls/Window.xaml
+++ b/src/Avalonia.Themes.Fluent/Controls/Window.xaml
@@ -15,9 +15,6 @@
           <Border Background="{TemplateBinding Background}" IsHitTestVisible="False" />
           <Panel Background="Transparent" Margin="{TemplateBinding WindowDecorationMargin}" />
           <VisualLayerManager>
-            <VisualLayerManager.ChromeOverlayLayer>
-              <TitleBar />
-            </VisualLayerManager.ChromeOverlayLayer>
             <ContentPresenter Name="PART_ContentPresenter"
                               ContentTemplate="{TemplateBinding ContentTemplate}"
                               Content="{TemplateBinding Content}"
diff --git a/src/Avalonia.Themes.Simple/Controls/Window.xaml b/src/Avalonia.Themes.Simple/Controls/Window.xaml
index 1a1c9f40cd..43eef2e515 100644
--- a/src/Avalonia.Themes.Simple/Controls/Window.xaml
+++ b/src/Avalonia.Themes.Simple/Controls/Window.xaml
@@ -18,9 +18,6 @@
           <Panel Margin="{TemplateBinding WindowDecorationMargin}"
                  Background="Transparent" />
           <VisualLayerManager>
-            <VisualLayerManager.ChromeOverlayLayer>
-              <TitleBar />
-            </VisualLayerManager.ChromeOverlayLayer>
             <ContentPresenter Name="PART_ContentPresenter"
                               Margin="{TemplateBinding Padding}"
                               HorizontalContentAlignment="{TemplateBinding HorizontalContentAlignment}"