diff --git a/src/Avalonia.Controls/ContextMenu.cs b/src/Avalonia.Controls/ContextMenu.cs
index 1735599988..86499530da 100644
--- a/src/Avalonia.Controls/ContextMenu.cs
+++ b/src/Avalonia.Controls/ContextMenu.cs
@@ -1,4 +1,5 @@
 using System;
+using System.Collections.Generic;
 using System.ComponentModel;
 using System.Linq;
 using Avalonia.Controls.Generators;
@@ -9,18 +10,19 @@ using Avalonia.Input;
 using Avalonia.Interactivity;
 using Avalonia.Layout;
 using Avalonia.LogicalTree;
+using Avalonia.Styling;
 
 namespace Avalonia.Controls
 {
     /// <summary>
     /// A control context menu.
     /// </summary>
-    public class ContextMenu : MenuBase
+    public class ContextMenu : MenuBase, ISetterValue
     {
         private static readonly ITemplate<IPanel> DefaultPanel =
             new FuncTemplate<IPanel>(() => new StackPanel { Orientation = Orientation.Vertical });
         private Popup _popup;
-        private Control _attachedControl;
+        private List<Control> _attachedControls;
         private IInputElement _previousFocus;
 
         /// <summary>
@@ -74,13 +76,14 @@ namespace Avalonia.Controls
             if (e.OldValue is ContextMenu oldMenu)
             {
                 control.PointerReleased -= ControlPointerReleased;
-                oldMenu._attachedControl = null;
+                oldMenu._attachedControls?.Remove(control);
                 ((ISetLogicalParent)oldMenu._popup)?.SetParent(null);
             }
 
             if (e.NewValue is ContextMenu newMenu)
             {
-                newMenu._attachedControl = control;
+                newMenu._attachedControls ??= new List<Control>();
+                newMenu._attachedControls.Add(control);
                 control.PointerReleased += ControlPointerReleased;
             }
         }
@@ -96,18 +99,22 @@ namespace Avalonia.Controls
         /// <param name="control">The control.</param>
         public void Open(Control control)
         {
-            if (control is null && _attachedControl is null)
+            if (control is null && (_attachedControls is null || _attachedControls.Count == 0))
             {
                 throw new ArgumentNullException(nameof(control));
             }
 
-            if (control is object && _attachedControl is object && control != _attachedControl)
+            if (control is object &&
+                _attachedControls is object &&
+                !_attachedControls.Contains(control))
             {
                 throw new ArgumentException(
                     "Cannot show ContentMenu on a different control to the one it is attached to.",
                     nameof(control));
             }
 
+            control ??= _attachedControls[0];
+
             if (IsOpen)
             {
                 return;
@@ -126,7 +133,12 @@ namespace Avalonia.Controls
                 _popup.Closed += PopupClosed;
             }
 
-            ((ISetLogicalParent)_popup).SetParent(control);
+            if (_popup.Parent != control)
+            {
+                ((ISetLogicalParent)_popup).SetParent(null);
+                ((ISetLogicalParent)_popup).SetParent(control);
+            }
+
             _popup.Child = this;
             _popup.IsOpen = true;
 
@@ -155,6 +167,17 @@ namespace Avalonia.Controls
             }
         }
 
+        void ISetterValue.Initialize(ISetter setter)
+        {
+            // ContextMenu can be assigned to the ContextMenu property in a setter. This overrides
+            // the behavior defined in Control which requires controls to be wrapped in a <template>.
+            if (!(setter is Setter s && s.Property == ContextMenuProperty))
+            {
+                throw new InvalidOperationException(
+                    "Cannot use a control as a Setter value. Wrap the control in a <Template>.");
+            }
+        }
+
         protected override IItemContainerGenerator CreateItemContainerGenerator()
         {
             return new MenuItemContainerGenerator(this);
@@ -179,7 +202,7 @@ namespace Avalonia.Controls
             SelectedIndex = -1;
             IsOpen = false;
 
-            if (_attachedControl is null)
+            if (_attachedControls is null || _attachedControls.Count == 0)
             {
                 ((ISetLogicalParent)_popup).SetParent(null);
             }
diff --git a/tests/Avalonia.Controls.UnitTests/ContextMenuTests.cs b/tests/Avalonia.Controls.UnitTests/ContextMenuTests.cs
index 28e87dd671..9a81d19bb9 100644
--- a/tests/Avalonia.Controls.UnitTests/ContextMenuTests.cs
+++ b/tests/Avalonia.Controls.UnitTests/ContextMenuTests.cs
@@ -1,7 +1,10 @@
 using System;
 using Avalonia.Input;
+using Avalonia.Markup.Xaml;
+using Avalonia.Markup.Xaml.MarkupExtensions;
 using Avalonia.Platform;
 using Avalonia.UnitTests;
+using Castle.DynamicProxy.Generators;
 using Moq;
 using Xunit;
 
@@ -168,6 +171,90 @@ namespace Avalonia.Controls.UnitTests
             }
         }
 
+        [Fact]
+        public void Context_Menu_In_Resources_Can_Be_Shared()
+        {
+            using (Application())
+            {
+                var xaml = @"
+<Window xmlns='https://github.com/avaloniaui'
+        xmlns:x='http://schemas.microsoft.com/winfx/2006/xaml'>
+    <Window.Resources>
+        <ContextMenu x:Key='contextMenu'>
+            <MenuItem>Foo</MenuItem>
+        </ContextMenu>
+	</Window.Resources>
+
+    <StackPanel>
+        <TextBlock Name='target1' ContextMenu='{StaticResource contextMenu}'/>
+        <TextBlock Name='target2' ContextMenu='{StaticResource contextMenu}'/>
+    </StackPanel>
+</Window>";
+
+                var loader = new AvaloniaXamlLoader();
+                var window = (Window)loader.Load(xaml);
+                var target1 = window.Find<TextBlock>("target1");
+                var target2 = window.Find<TextBlock>("target2");
+                var mouse = new MouseTestHelper();
+
+                Assert.NotNull(target1.ContextMenu);
+                Assert.NotNull(target2.ContextMenu);
+                Assert.Same(target1.ContextMenu, target2.ContextMenu);
+
+                window.Show();
+
+                var menu = target1.ContextMenu;
+                mouse.Click(target1, MouseButton.Right);
+                Assert.True(menu.IsOpen);
+                mouse.Click(target2, MouseButton.Right);
+                Assert.True(menu.IsOpen);
+            }
+        }
+
+        [Fact]
+        public void Context_Menu_Can_Be_Set_In_Style()
+        {
+            using (Application())
+            {
+                var xaml = @"
+<Window xmlns='https://github.com/avaloniaui'
+        xmlns:x='http://schemas.microsoft.com/winfx/2006/xaml'>
+    <Window.Styles>
+        <Style Selector='TextBlock'>
+            <Setter Property='ContextMenu'>
+                <ContextMenu>
+                    <MenuItem>Foo</MenuItem>
+                </ContextMenu>
+            </Setter>
+        </Style>
+	</Window.Styles>
+
+    <StackPanel>
+        <TextBlock Name='target1'/>
+        <TextBlock Name='target2'/>
+    </StackPanel>
+</Window>";
+
+                var loader = new AvaloniaXamlLoader();
+                var window = (Window)loader.Load(xaml);
+                var target1 = window.Find<TextBlock>("target1");
+                var target2 = window.Find<TextBlock>("target2");
+                var mouse = new MouseTestHelper();
+
+                Assert.NotNull(target1.ContextMenu);
+                Assert.NotNull(target2.ContextMenu);
+                Assert.Same(target1.ContextMenu, target2.ContextMenu);
+
+                window.Show();
+
+                var menu = target1.ContextMenu;
+                mouse.Click(target1, MouseButton.Right);
+                Assert.True(menu.IsOpen);
+                mouse.Click(target2, MouseButton.Right);
+                Assert.True(menu.IsOpen);
+            }
+        }
+
         [Fact(Skip = "The only reason this test was 'passing' before was that the author forgot to call Window.ApplyTemplate()")]
         public void Cancelling_Closing_Leaves_ContextMenuOpen()
         {