diff --git a/src/Avalonia.Controls/Primitives/LightDismissOverlayLayer.cs b/src/Avalonia.Controls/Primitives/LightDismissOverlayLayer.cs
index 4662d2532e..da51cdf1e7 100644
--- a/src/Avalonia.Controls/Primitives/LightDismissOverlayLayer.cs
+++ b/src/Avalonia.Controls/Primitives/LightDismissOverlayLayer.cs
@@ -1,5 +1,7 @@
 using System;
+using System.Collections.Generic;
 using System.Linq;
+using System.Threading;
 using Avalonia.Controls.Templates;
 using Avalonia.Input;
 using Avalonia.Media;
@@ -14,11 +16,14 @@ namespace Avalonia.Controls.Primitives
     /// </summary>
     internal class LightDismissOverlayLayer : Border, ICustomHitTest
     {
-        public IInputElement? InputPassThroughElement { get; set; }
+        private readonly List<Registration> _registrations = [];
+
+        public IInputElement? InputPassThroughElement => _registrations.LastOrDefault()?.InputPassThroughElement;
 
         static LightDismissOverlayLayer()
         {
             BackgroundProperty.OverrideDefaultValue<LightDismissOverlayLayer>(Brushes.Transparent);
+            IsVisibleProperty.OverrideDefaultValue<LightDismissOverlayLayer>(false);
         }
 
         /// <summary>
@@ -46,6 +51,14 @@ namespace Avalonia.Controls.Primitives
             return manager?.LightDismissOverlayLayer;
         }
 
+        public IDisposable Register(IInputElement? inputPassThroughElement)
+        {
+            var registration = new Registration(this, inputPassThroughElement);
+            _registrations.Add(registration);
+            UpdateState();
+            return registration;
+        }
+
         /// <inheritdoc />
         public bool HitTest(Point point)
         {
@@ -59,5 +72,30 @@ namespace Avalonia.Controls.Primitives
 
             return true;
         }
+
+        private void Unregister(Registration registration)
+        {
+            _registrations.Remove(registration);
+            UpdateState();
+        }
+
+        private void UpdateState()
+        {
+            IsVisible = _registrations.Count > 0;
+        }
+
+        private sealed class Registration(LightDismissOverlayLayer owner, IInputElement? inputPassThroughElement) : IDisposable
+        {
+            private LightDismissOverlayLayer? _owner = owner;
+
+            public IInputElement? InputPassThroughElement { get; } = inputPassThroughElement;
+
+            public void Dispose()
+            {
+                var owner = _owner;
+                _owner = null;
+                owner?.Unregister(this);
+            }
+        }
     }
 }
diff --git a/src/Avalonia.Controls/Primitives/Popup.cs b/src/Avalonia.Controls/Primitives/Popup.cs
index ba9ca5b572..46ab0b391a 100644
--- a/src/Avalonia.Controls/Primitives/Popup.cs
+++ b/src/Avalonia.Controls/Primitives/Popup.cs
@@ -565,14 +565,7 @@ namespace Avalonia.Controls.Primitives
 
                 if (dismissLayer != null)
                 {
-                    dismissLayer.IsVisible = true;
-                    dismissLayer.InputPassThroughElement = OverlayInputPassThroughElement;
-                    
-                    Disposable.Create(() =>
-                    {
-                        dismissLayer.IsVisible = false;
-                        dismissLayer.InputPassThroughElement = null;
-                    }).DisposeWith(handlerCleanup);
+                    dismissLayer.Register(OverlayInputPassThroughElement).DisposeWith(handlerCleanup);
                     
                     SubscribeToEventHandler<LightDismissOverlayLayer, EventHandler<PointerPressedEventArgs>>(
                         dismissLayer,
diff --git a/src/Avalonia.Controls/Primitives/VisualLayerManager.cs b/src/Avalonia.Controls/Primitives/VisualLayerManager.cs
index fd5c55ef62..573926d2cc 100644
--- a/src/Avalonia.Controls/Primitives/VisualLayerManager.cs
+++ b/src/Avalonia.Controls/Primitives/VisualLayerManager.cs
@@ -109,10 +109,7 @@ namespace Avalonia.Controls.Primitives
                 var rv = FindLayer<LightDismissOverlayLayer>();
                 if (rv == null)
                 {
-                    rv = new LightDismissOverlayLayer
-                    {
-                        IsVisible = false
-                    };
+                    rv = new LightDismissOverlayLayer();
 
                     AddLayer(rv, LightDismissOverlayZIndex);
                 }
diff --git a/tests/Avalonia.Controls.UnitTests/Primitives/PopupTests.cs b/tests/Avalonia.Controls.UnitTests/Primitives/PopupTests.cs
index 3548cd614f..c06ed62a5c 100644
--- a/tests/Avalonia.Controls.UnitTests/Primitives/PopupTests.cs
+++ b/tests/Avalonia.Controls.UnitTests/Primitives/PopupTests.cs
@@ -1391,6 +1391,41 @@ namespace Avalonia.Controls.UnitTests.Primitives
                 Assert.Equal(true, target.IsUsingOverlayLayer);
             }
         }
+        
+        [Fact]
+        public void Closing_Previous_Light_Dismiss_Popup_Should_Not_Affect_Overlay_For_Next_Popup()
+        {
+            using (CreateServices())
+            {
+                var placementTarget = new Border();
+                var window = PreparedWindow(placementTarget);
+                var first = new Popup
+                {
+                    PlacementTarget = placementTarget,
+                    IsLightDismissEnabled = true,
+                };
+                var second = new Popup
+                {
+                    PlacementTarget = placementTarget,
+                    IsLightDismissEnabled = true,
+                };
+
+                first.Open();
+                second.Open();
+
+                var overlay = LightDismissOverlayLayer.GetLightDismissOverlayLayer(window);
+                Assert.NotNull(overlay);
+
+                first.Close();
+
+                Assert.True(overlay.IsVisible);
+
+                overlay.RaiseEvent(CreatePointerPressedEventArgs(window, new Point(10, 15)));
+
+                Assert.False(second.IsOpen);
+                Assert.False(overlay.IsVisible);
+            }
+        }
 
         [Fact]
         public void Opened_Popup_Should_Be_In_OpenedPopups()