diff --git a/src/Avalonia.Controls/Design.cs b/src/Avalonia.Controls/Design.cs
index 80600b2276..9d6bb93ebb 100644
--- a/src/Avalonia.Controls/Design.cs
+++ b/src/Avalonia.Controls/Design.cs
@@ -1,102 +1,433 @@
-
+using System;
 using System.Collections.Generic;
-using System.Runtime.CompilerServices;
+using Avalonia.Controls.Templates;
+using Avalonia.Layout;
+using Avalonia.Metadata;
 using Avalonia.Styling;
 
 namespace Avalonia.Controls
 {
+    /// <summary>
+    /// Provides attached properties and helpers for design-time support.
+    /// </summary>
     public static class Design
     {
-        private static Dictionary<object, Control?>? _previewWith;
+        private static Dictionary<object, ITemplate<Control>?> s_previewWith = [];
+        private static Dictionary<object, object?> s_templateDataContext = [];
 
+        /// <summary>
+        /// Gets a value indicating whether the application is running in design mode.
+        /// </summary>
+        /// <remarks>
+        /// This property is typically used to enable or disable features that should only be available
+        /// at design-time, such as sample/preview data.
+        /// </remarks>
         public static bool IsDesignMode { get; internal set; }
 
+        /// <summary>
+        /// Defines the Height attached property.
+        /// </summary>
         public static readonly AttachedProperty<double> HeightProperty = AvaloniaProperty
             .RegisterAttached<Control, double>("Height", typeof (Design));
 
+        /// <summary>
+        /// Sets the design-time height for a control.
+        /// </summary>
+        /// <param name="control">The control to set the height for.</param>
+        /// <param name="value">The height value.</param>
         public static void SetHeight(Control control, double value)
         {
             control.SetValue(HeightProperty, value);
         }
 
+        /// <summary>
+        /// Gets the design-time height for a control.
+        /// </summary>
+        /// <param name="control">The control to get the height from.</param>
+        /// <returns>The height value.</returns>
         public static double GetHeight(Control control)
         {
             return control.GetValue(HeightProperty);
         }
 
+        /// <summary>
+        /// Defines the Width attached property.
+        /// </summary>
         public static readonly AttachedProperty<double> WidthProperty = AvaloniaProperty
             .RegisterAttached<Control, double>("Width", typeof(Design));
 
+        /// <summary>
+        /// Sets the design-time width for a control.
+        /// </summary>
+        /// <param name="control">The control to set the width for.</param>
+        /// <param name="value">The width value.</param>
         public static void SetWidth(Control control, double value)
         {
             control.SetValue(WidthProperty, value);
         }
 
+        /// <summary>
+        /// Gets the design-time width for a control.
+        /// </summary>
+        /// <param name="control">The control to get the width from.</param>
+        /// <returns>The width value.</returns>
         public static double GetWidth(Control control)
         {
             return control.GetValue(WidthProperty);
         }
 
-        public static readonly AttachedProperty<object> DataContextProperty = AvaloniaProperty
-            .RegisterAttached<Control, object>("DataContext", typeof (Design));
+        /// <summary>
+        /// Defines the DataContext attached property.
+        /// </summary>
+        public static readonly AttachedProperty<object?> DataContextProperty = AvaloniaProperty
+            .RegisterAttached<Control, object?>("DataContext", typeof (Design));
 
-        public static void SetDataContext(Control control, object value)
+        /// <summary>
+        /// Sets the design-time data context for a control.
+        /// </summary>
+        /// <param name="control">The control to set the data context for.</param>
+        /// <param name="value">The data context value.</param>
+        public static void SetDataContext(Control control, object? value)
         {
             control.SetValue(DataContextProperty, value);
         }
 
-        public static object GetDataContext(Control control)
+        /// <summary>
+        /// Gets the design-time data context for a control.
+        /// </summary>
+        /// <param name="control">The control to get the data context from.</param>
+        /// <returns>The data context value.</returns>
+        public static object? GetDataContext(Control control)
         {
             return control.GetValue(DataContextProperty);
         }
-        
+
+        /// <summary>
+        /// Sets the design-time data context for a control.
+        /// </summary>
+        /// <param name="control">The control to set the data context for.</param>
+        /// <param name="value">The data context value.</param>
+        public static void SetDataContext(IDataTemplate control, object? value)
+        {
+            s_templateDataContext[control] = value;
+        }
+
+        /// <summary>
+        /// Gets the design-time data context for a control.
+        /// </summary>
+        /// <param name="control">The control to get the data context from.</param>
+        /// <returns>The data context value.</returns>
+        public static object? GetDataContext(IDataTemplate control)
+        {
+            return s_templateDataContext.TryGetValue(control, out var value) ? value : null;
+        }
+
+        /// <summary>
+        /// Defines the PreviewWith attached property.
+        /// </summary>
         public static readonly AttachedProperty<Control?> PreviewWithProperty = AvaloniaProperty
             .RegisterAttached<AvaloniaObject, Control?>("PreviewWith", typeof (Design));
 
+        /// <summary>
+        /// Sets a preview template for the specified <see cref="AvaloniaObject"/> at design-time.
+        /// </summary>
+        /// <remarks>
+        /// This method allows you to specify a substitute control to be rendered in the previewer
+        /// for a given object.
+        /// </remarks>
+        /// <param name="target">The target object.</param>
+        /// <param name="control">The preview control.</param>
+        // TODO12: Remove this overload in Avalonia 12
+        [Obsolete("Use SetPreviewWith(AvaloniaObject, ITemplate<Control>) overload instead. Use <Template></Template> from XAML")]
         public static void SetPreviewWith(AvaloniaObject target, Control? control)
         {
-            target.SetValue(PreviewWithProperty, control);
+            s_previewWith[target] = control is not null ? new FuncTemplate<Control>(() => control) : null;
+        }
+    
+        /// <summary>
+        /// Sets a preview template for the specified <see cref="AvaloniaObject"/> at design-time.
+        /// </summary>
+        /// <remarks>
+        /// This method allows you to specify a substitute control template to be rendered in the previewer
+        /// for a given object.
+        /// </remarks>
+        /// <param name="target">The target object.</param>
+        /// <param name="template">The preview template.</param>
+        public static void SetPreviewWith(AvaloniaObject target, ITemplate<Control>? template)
+        {
+            s_previewWith[target] = template;
         }
 
+        /// <summary>
+        /// Sets a preview template for the specified <see cref="ResourceDictionary"/> at design-time.
+        /// </summary>
+        /// <remarks>
+        /// This method allows you to specify a substitute control template to be rendered in the previewer.
+        /// ResourceDictionary is attached to that control, displaying real time changes on the control. 
+        /// </remarks>
+        /// <param name="target">The resource dictionary.</param>
+        /// <param name="template">The preview template.</param>
+        public static void SetPreviewWith(ResourceDictionary target, ITemplate<Control>? template)
+        {
+            s_previewWith[target] = template;
+        } 
+
+        /// <summary>
+        /// Sets a preview template for the specified <see cref="ResourceDictionary"/> at design-time.
+        /// </summary>
+        /// <remarks>
+        /// This method allows you to specify a substitute control to be rendered in the previewer.
+        /// ResourceDictionary is attached to that control, displaying real time changes on the control. 
+        /// </remarks>
+        /// <param name="target">The resource dictionary.</param>
+        /// <param name="control">The preview control.</param>
         public static void SetPreviewWith(ResourceDictionary target, Control? control)
         {
-            _previewWith ??= new();
-            _previewWith[target] = control;
+            s_previewWith[target] = control is not null ? new FuncTemplate<Control>(() => control) : null;
+        } 
+
+        /// <summary>
+        /// Sets a preview template for the specified <see cref="IDataTemplate"/> at design-time.
+        /// </summary>
+        /// <remarks>
+        /// This method allows you to specify a substitute control template to be rendered in the previewer.
+        /// Template must return ContentControl, and IDataTemplate will be set assigned to ContentControl.ContentTemplate property.
+        /// </remarks>
+        /// <param name="target">The data template.</param>
+        /// <param name="template">The preview template.</param>
+        public static void SetPreviewWith(IDataTemplate target, ITemplate<Control>? template)
+        {
+            s_previewWith[target] = template is not null ? new FuncTemplate<Control>(template.Build) : null;
+        }
+
+        /// <summary>
+        /// Sets a preview template for the specified <see cref="IDataTemplate"/> at design-time.
+        /// </summary>
+        /// <remarks>
+        /// This method allows you to specify a substitute control to be rendered in the previewer.
+        /// Template must return ContentControl, and IDataTemplate will be set assigned to ContentControl.ContentTemplate property.
+        /// </remarks>
+        /// <param name="target">The data template.</param>
+        /// <param name="control">The preview control.</param>
+        public static void SetPreviewWith(IDataTemplate target, Control? control)
+        {
+            s_previewWith[target] = control is not null ? new FuncTemplate<Control>(() => control) : null;
+        }
+
+        
+        /// <summary>
+        /// Sets a preview template for the specified <see cref="IDataTemplate"/> at design-time.
+        /// </summary>
+        /// <remarks>
+        /// This method allows you to specify a substitute control template to be rendered in the previewer.
+        /// Template must return ContentControl, and IDataTemplate will be set assigned to ContentControl.ContentTemplate property.
+        /// </remarks>
+        /// <param name="target">The data template.</param>
+        /// <param name="template">The preview template.</param>
+        public static void SetPreviewWith(IStyle target, ITemplate<Control>? template)
+        {
+            s_previewWith[target] = template is not null ? new FuncTemplate<Control>(template.Build) : null;
+        }
+
+        
+        /// <summary>
+        /// Sets a preview template for the specified <see cref="IDataTemplate"/> at design-time.
+        /// </summary>
+        /// <remarks>
+        /// This method allows you to specify a substitute control to be rendered in the previewer.
+        /// Template must return ContentControl, and IDataTemplate will be set assigned to ContentControl.ContentTemplate property.
+        /// </remarks>
+        /// <param name="target">The data template.</param>
+        /// <param name="control">The preview control.</param>
+        public static void SetPreviewWith(IStyle target, Control? control)
+        {
+            s_previewWith[target] = control is not null ? new FuncTemplate<Control>(() => control) : null;
         }
 
+        
+        /// <summary>
+        /// Gets the preview control for the specified <see cref="AvaloniaObject"/> at design-time.
+        /// </summary>
+        /// <param name="target">The target object.</param>
+        /// <returns>The preview control, or null.</returns>
         public static Control? GetPreviewWith(AvaloniaObject target)
         {
-            return target.GetValue(PreviewWithProperty);
+            return s_previewWith.TryGetValue(target, out var template) ? template?.Build() : null;
         }
 
+        /// <summary>
+        /// Gets the preview control for the specified <see cref="ResourceDictionary"/> at design-time.
+        /// </summary>
+        /// <param name="target">The resource dictionary.</param>
+        /// <returns>The preview control, or null.</returns>
         public static Control? GetPreviewWith(ResourceDictionary target)
         {
-            return _previewWith?[target];
+            return s_previewWith.TryGetValue(target, out var template) ? template?.Build() : null;
+        }
+
+        /// <summary>
+        /// Gets the preview control for the specified <see cref="IDataTemplate"/> at design-time.
+        /// </summary>
+        /// <param name="target">The data template.</param>
+        /// <returns>The preview control, or null.</returns>
+        public static Control? GetPreviewWith(IDataTemplate target)
+        {
+            return s_previewWith.TryGetValue(target, out var template) ? template?.Build() : null;
+        }
+
+        /// <summary>
+        /// Gets the preview control for the specified <see cref="IStyle"/> at design-time.
+        /// </summary>
+        /// <param name="target">The style.</param>
+        /// <returns>The preview control, or null.</returns>
+        public static Control? GetPreviewWith(IStyle target)
+        {
+            return s_previewWith.TryGetValue(target, out var template) ? template?.Build() : null;
         }
 
+        /// <summary>
+        /// Identifies the DesignStyle attached property for design-time use.
+        /// </summary>
+        /// <remarks>
+        /// This property allows you to apply a style to a control only at design-time, enabling
+        /// custom visualizations or highlighting in the designer without affecting the runtime appearance.
+        /// </remarks>
         public static readonly AttachedProperty<IStyle> DesignStyleProperty = AvaloniaProperty
             .RegisterAttached<Control, IStyle>("DesignStyle", typeof(Design));
 
+        /// <summary>
+        /// Sets the design-time style for a control.
+        /// </summary>
+        /// <param name="control">The control to set the style for.</param>
+        /// <param name="value">The style value.</param>
         public static void SetDesignStyle(Control control, IStyle value)
         {
             control.SetValue(DesignStyleProperty, value);
         }
 
+        /// <summary>
+        /// Gets the design-time style for a control.
+        /// </summary>
+        /// <param name="control">The control to get the style from.</param>
+        /// <returns>The style value.</returns>
         public static IStyle GetDesignStyle(Control control)
         {
             return control.GetValue(DesignStyleProperty);
         }
 
+        [PrivateApi]
         public static void ApplyDesignModeProperties(Control target, Control source)
         {
             if (source.IsSet(WidthProperty))
-                target.Width = source.GetValue(WidthProperty);
+                target.Bind(Layoutable.WidthProperty, target.GetBindingObservable(WidthProperty));
             if (source.IsSet(HeightProperty))
-                target.Height = source.GetValue(HeightProperty);
+                target.Bind(Layoutable.HeightProperty, target.GetBindingObservable(HeightProperty));
             if (source.IsSet(DataContextProperty))
-                target.DataContext = source.GetValue(DataContextProperty);
+                target.Bind(StyledElement.DataContextProperty, target.GetBindingObservable(DataContextProperty));
             if (source.IsSet(DesignStyleProperty))
-                target.Styles.Add(source.GetValue(DesignStyleProperty));
+                target.Styles.Add(GetDesignStyle(source));
+        }
+
+        [PrivateApi]
+        public static Control CreatePreviewWithControl(object target)
+        {
+            if (target is IStyle style)
+            {
+                var substitute = GetPreviewWith((AvaloniaObject)style);
+                if (substitute != null)
+                {
+                    substitute.Styles.Add(style);
+                    return substitute;
+                }
+
+                return new StackPanel
+                {
+                    Children =
+                    {
+                        new TextBlock {Text = "Styles can't be previewed without Design.PreviewWith. Add"},
+                        new TextBlock {Text = "<Design.PreviewWith>"},
+                        new TextBlock {Text = "    <Border Padding=\"20\"><!-- YOUR CONTROL FOR PREVIEW HERE --></Border>"},
+                        new TextBlock {Text = "</Design.PreviewWith>"},
+                        new TextBlock {Text = "before setters in your first Style"}
+                    }
+                };
+            }
+
+            if (target is ResourceDictionary resources)
+            {
+                var substitute = GetPreviewWith(resources);
+                if (substitute != null)
+                {
+                    substitute.Resources.MergedDictionaries.Add(resources);
+                    return substitute;
+                }
+
+                return new StackPanel
+                {
+                    Children =
+                    {
+                        new TextBlock {Text = "ResourceDictionaries can't be previewed without Design.PreviewWith. Add"},
+                        new TextBlock {Text = "<Design.PreviewWith>"},
+                        new TextBlock {Text = "    <Border Padding=\"20\"><!-- YOUR CONTROL FOR PREVIEW HERE --></Border>"},
+                        new TextBlock {Text = "</Design.PreviewWith>"},
+                        new TextBlock {Text = "in your resource dictionary"}
+                    }
+                };
+            }
+
+            if (target is IDataTemplate template)
+            {
+                if (GetPreviewWith(template) is ContentControl substitute)
+                {
+                    substitute.ContentTemplate = template;
+                    if (!substitute.IsSet(DataContextProperty) && substitute.IsSet(StyledElement.DataContextProperty))
+                    {
+                        substitute.DataContext = substitute.GetValue(StyledElement.DataContextProperty);
+                    }
+                    return substitute;
+                }
+
+                if (GetDataContext(template) is { } dataContext)
+                {
+                    substitute = new ContentControl
+                    {
+                        ContentTemplate = template,
+                        DataContext = dataContext,
+                        Content = dataContext
+                    };
+                    return substitute;
+                }
+
+                return new StackPanel
+                {
+                    Children =
+                    {
+                        new TextBlock {Text = "IDataTemplate can't be previewed without Design.PreviewWith."},
+                        new TextBlock {Text = "Provide ContentControl with your design data as Content. Previewer will set ContentTemplate from this file."},
+                        new TextBlock {Text = "<Design.PreviewWith>"},
+                        new TextBlock {Text = "    <ContentControl Content=\"{x:Static YOUR_DATA_OBJECT_HERE}\" />"},
+                        new TextBlock {Text = "</Design.PreviewWith>"}
+                    }
+                };
+            }
+
+            if (target is Application)
+            {
+                return new TextBlock { Text = "This file cannot be previewed in design view" };
+            }
+
+            if (target is AvaloniaObject avObject and not Window
+                && GetPreviewWith(avObject) is { } previewWith)
+            {
+                return previewWith;
+            }
+
+            if (target is not Control control)
+            {
+                return new TextBlock { Text = "This file cannot be previewed in design view" };
+            }
+
+            return control;
         }
     }
 }
diff --git a/src/Avalonia.DesignerSupport/DesignWindowLoader.cs b/src/Avalonia.DesignerSupport/DesignWindowLoader.cs
index 6395529278..df6d7abd4d 100644
--- a/src/Avalonia.DesignerSupport/DesignWindowLoader.cs
+++ b/src/Avalonia.DesignerSupport/DesignWindowLoader.cs
@@ -6,6 +6,7 @@ using System.Text;
 using Avalonia.Controls;
 using Avalonia.Controls.Embedding.Offscreen;
 using Avalonia.Controls.Platform;
+using Avalonia.Controls.Templates;
 using Avalonia.Markup.Xaml;
 using Avalonia.Styling;
 
@@ -19,7 +20,6 @@ namespace Avalonia.DesignerSupport
         public static Window LoadDesignerWindow(string xaml, string assemblyPath, string xamlFileProjectPath, double renderScaling)
         {
             Window window;
-            Control control;
             using (PlatformManager.DesignerMode())
             {
                 var loader = AvaloniaLocator.Current.GetRequiredService<AvaloniaXamlLoader.IRuntimeXamlLoader>();
@@ -45,60 +45,9 @@ namespace Avalonia.DesignerSupport
                     DesignMode = true,
                     UseCompiledBindingsByDefault = bool.TryParse(useCompiledBindings, out var parsedValue) && parsedValue
                 });
-                var style = loaded as IStyle;
-                var resources = loaded as ResourceDictionary;
-                if (style != null)
-                {
-                    var substitute = Design.GetPreviewWith((AvaloniaObject)style);
-                    if (substitute != null)
-                    {
-                        substitute.Styles.Add(style);
-                        control = substitute;
-                    }
-                    else
-                        control = new StackPanel
-                        {
-                            Children =
-                            {
-                                new TextBlock {Text = "Styles can't be previewed without Design.PreviewWith. Add"},
-                                new TextBlock {Text = "<Design.PreviewWith>"},
-                                new TextBlock {Text = "    <Border Padding=20><!-- YOUR CONTROL FOR PREVIEW HERE --></Border>"},
-                                new TextBlock {Text = "</Design.PreviewWith>"},
-                                new TextBlock {Text = "before setters in your first Style"}
-                            }
-                        };
-                }
-                else if (resources != null)
-                {
-                    var substitute = Design.GetPreviewWith(resources);
-                    if (substitute != null)
-                    {
-                        substitute.Resources.MergedDictionaries.Add(resources);
-                        control = substitute;
-                    }
-                    else
-                        control = new StackPanel
-                        {
-                            Children =
-                            {
-                                new TextBlock {Text = "ResourceDictionaries can't be previewed without Design.PreviewWith. Add"},
-                                new TextBlock {Text = "<Design.PreviewWith>"},
-                                new TextBlock {Text = "    <Border Padding=20><!-- YOUR CONTROL FOR PREVIEW HERE --></Border>"},
-                                new TextBlock {Text = "</Design.PreviewWith>"},
-                                new TextBlock {Text = "in your resource dictionary"}
-                            }
-                        };
-                }
-                else if (loaded is Application)
-                    control = new TextBlock { Text = "This file cannot be previewed in design view" };
-                else
-                    control = (Control)loaded;
 
-                window = control as Window;
-                if (window == null)
-                {
-                    window = new Window() { Content = (Control)control };
-                }
+                var control = Design.CreatePreviewWithControl(loaded);
+                window = control as Window ?? new Window { Content = control };
 
                 if (window.PlatformImpl is OffscreenTopLevelImplBase offscreenImpl)
                     offscreenImpl.RenderScaling = renderScaling;
diff --git a/tests/Avalonia.Controls.UnitTests/DesignTests.cs b/tests/Avalonia.Controls.UnitTests/DesignTests.cs
new file mode 100644
index 0000000000..6845e4d369
--- /dev/null
+++ b/tests/Avalonia.Controls.UnitTests/DesignTests.cs
@@ -0,0 +1,149 @@
+using Avalonia.Controls.Templates;
+using Avalonia.LogicalTree;
+using Avalonia.Markup.Xaml.MarkupExtensions;
+using Avalonia.Media;
+using Avalonia.UnitTests;
+using Avalonia.Styling;
+using System;
+using System.Linq;
+using Avalonia.Controls.Primitives;
+using Xunit;
+
+namespace Avalonia.Controls.UnitTests;
+
+public class DesignTests : ScopedTestBase
+{
+    [Fact]
+    public void Should_Preview_Resource_Dictionary_With_Template()
+    {
+        using var _ = UnitTestApplication.Start(TestServices.StyledWindow);
+
+        var dictionary = new ResourceDictionary { ["TestColor"] = Colors.Green };
+        Design.SetPreviewWith(dictionary,
+            new FuncTemplate<Control>(static () =>
+                new Border { [!Border.BackgroundProperty] = new DynamicResourceExtension("TestColor") }));
+
+        var preview = Design.CreatePreviewWithControl(dictionary);
+
+        var border = Assert.IsType<Border>(preview);
+        Assert.Equal(Colors.Green, ((ISolidColorBrush)border.Background!).Color);
+    }
+
+    [Fact]
+    public void Should_Preview_DataTemplate_With_ContentControl()
+    {
+        using var _ = UnitTestApplication.Start(TestServices.StyledWindow);
+
+        const string testData = "Test Data";
+        var dataTemplate = new FuncDataTemplate<string>((data, _) =>
+            new TextBlock { Text = data });
+        Design.SetPreviewWith(dataTemplate,
+            new FuncTemplate<Control>(static () => new ContentControl { Content = testData }));
+
+        var preview = Design.CreatePreviewWithControl(dataTemplate);
+
+        var previewContentControl = Assert.IsType<ContentControl>(preview);
+        Assert.Equal(testData, previewContentControl.Content);
+        Assert.Same(dataTemplate, previewContentControl.ContentTemplate);
+    }
+
+    [Fact]
+    public void Should_Preview_DataTemplate_With_DataContext()
+    {
+        using var _ = UnitTestApplication.Start(TestServices.StyledWindow);
+
+        const string testData = "Test Data";
+        var dataTemplate = new FuncDataTemplate<string>((data, _) =>
+            new TextBlock { Text = data });
+        Design.SetDataContext(dataTemplate, testData);
+
+        var preview = Design.CreatePreviewWithControl(dataTemplate);
+
+        var previewContentControl = Assert.IsType<ContentControl>(preview);
+        Assert.Equal(testData, previewContentControl.Content);
+        Assert.Same(dataTemplate, previewContentControl.ContentTemplate);
+    }
+
+    [Fact]
+    public void Should_Preview_Control_With_Another_Control()
+    {
+        using var _ = UnitTestApplication.Start(TestServices.StyledWindow);
+
+        var control = new TextBlock();
+        Design.SetPreviewWith(control,
+            new FuncTemplate<Control>(static () => new Border()));
+
+        var preview = Design.CreatePreviewWithControl(control);
+
+        Assert.IsType<Border>(preview);
+    }
+
+    [Fact]
+    public void Should_Apply_Design_Mode_Properties()
+    {
+        using var _ = UnitTestApplication.Start(TestServices.StyledWindow);
+
+        var control = new ContentControl();
+
+        Design.SetWidth(control, 200);
+        Design.SetHeight(control, 150);
+        Design.SetDataContext(control, "TestDataContext");
+        Design.SetDesignStyle(control,
+            new Style(x => x.OfType<ContentControl>())
+            {
+                Setters = { new Setter(TemplatedControl.BackgroundProperty, Brushes.Yellow) }
+            });
+
+        Design.ApplyDesignModeProperties(control, control);
+
+        Assert.Equal(200, control.Width);
+        Assert.Equal(150, control.Height);
+        Assert.Equal("TestDataContext", control.DataContext);
+        Assert.Contains(control.Styles,
+            s => ((Style)s).Setters.OfType<Setter>().First().Property == TemplatedControl.BackgroundProperty);
+    }
+
+    [Fact]
+    public void Should_Not_Throw_Exception_On_Generic_Style()
+    {
+        using var _ = UnitTestApplication.Start(TestServices.StyledWindow);
+
+        var preview = Design.CreatePreviewWithControl(new Style(x => x.OfType<Button>()));
+
+        // We are not going to test specific content of the placeholder preview control.
+        // But it should not throw and should not return null at least.
+        Assert.NotNull(preview);
+    }
+
+    [Fact]
+    public void Should_Not_Throw_Exception_On_Generic_Resource_Dictionary()
+    {
+        using var _ = UnitTestApplication.Start(TestServices.StyledWindow);
+
+        var preview = Design.CreatePreviewWithControl(new ResourceDictionary());
+
+        Assert.NotNull(preview);
+    }
+
+    [Fact]
+    public void Should_Not_Throw_Exception_On_Generic_Data_Template()
+    {
+        using var _ = UnitTestApplication.Start(TestServices.StyledWindow);
+
+        var preview = Design.CreatePreviewWithControl(new FuncDataTemplate<string>((data, _) =>
+            new TextBlock { Text = data }));
+
+        Assert.NotNull(preview);
+    }
+
+    [Fact]
+    public void Should_Not_Throw_Exception_On_Application()
+    {
+        using var _ = UnitTestApplication.Start(TestServices.StyledWindow);
+
+        var app = new Application();
+        var preview = Design.CreatePreviewWithControl(app);
+
+        Assert.NotNull(preview);
+    }
+}
diff --git a/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/BasicTests.cs b/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/BasicTests.cs
index 5875f2777d..2b93f64330 100644
--- a/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/BasicTests.cs
+++ b/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/BasicTests.cs
@@ -825,44 +825,6 @@ namespace Avalonia.Markup.Xaml.UnitTests.Xaml
             }
         }
 
-        [Fact]
-        public void Design_Mode_Properties_Should_Be_Ignored_At_Runtime_And_Set_In_Design_Mode()
-        {
-            using (UnitTestApplication.Start(TestServices.MockWindowingPlatform))
-            {
-                var xaml = @"
-<Window xmlns='https://github.com/avaloniaui' 
-    xmlns:d='http://schemas.microsoft.com/expression/blend/2008'
-    xmlns:mc='http://schemas.openxmlformats.org/markup-compatibility/2006'
-    mc:Ignorable='d'
-    d:DataContext='data-context'
-    d:DesignWidth='123'
-    d:DesignHeight='321'
->
-
-</Window>";
-                foreach (var designMode in new[] {true, false})
-                {
-                    var obj = (Window)AvaloniaRuntimeXamlLoader.Load(xaml, designMode: designMode);
-                    var context = Design.GetDataContext(obj);
-                    var width = Design.GetWidth(obj);
-                    var height = Design.GetHeight(obj);
-                    if (designMode)
-                    {
-                        Assert.Equal("data-context", context);
-                        Assert.Equal(123, width);
-                        Assert.Equal(321, height);
-                    }
-                    else
-                    {
-                        Assert.False(obj.IsSet(Design.DataContextProperty));
-                        Assert.False(obj.IsSet(Design.WidthProperty));
-                        Assert.False(obj.IsSet(Design.HeightProperty));
-                    }
-                }
-            }
-        }
-
         [Fact]
         public void Slider_Properties_Can_Be_Set_In_Any_Order()
         {
diff --git a/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/DesignModeTests.cs b/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/DesignModeTests.cs
new file mode 100644
index 0000000000..71f695c176
--- /dev/null
+++ b/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/DesignModeTests.cs
@@ -0,0 +1,193 @@
+using System;
+using Avalonia.Controls;
+using Avalonia.Markup.Xaml.Templates;
+using Avalonia.Media;
+using Avalonia.Styling;
+using Avalonia.UnitTests;
+using Avalonia.VisualTree;
+using Xunit;
+
+namespace Avalonia.Markup.Xaml.UnitTests.Xaml;
+
+public class DesignModeTests : XamlTestBase
+{
+    public static object SomeStaticProperty { get; set; }
+
+    [Fact]
+    public void Design_Mode_PreviewWith_Should_Be_Ignored_Without_Design_Mode()
+    {
+        using (UnitTestApplication.Start(TestServices.MockWindowingPlatform))
+        {
+            var obj = (Control)AvaloniaRuntimeXamlLoader.Load(@"
+<Button xmlns='https://github.com/avaloniaui'>
+    <Design.PreviewWith>
+        <Template>
+            <Border />
+        </Template>
+    </Design.PreviewWith>
+</Button>", designMode: false);
+            var preview = Design.CreatePreviewWithControl(obj);
+            // Should return the original control, not the preview.
+            Assert.IsType<Button>(preview);
+        }
+    }
+
+    [Fact]
+    public void Design_Mode_PreviewWith_Works_With_Control_Template()
+    {
+        using (UnitTestApplication.Start(TestServices.MockWindowingPlatform))
+        {
+            var obj = (Control)AvaloniaRuntimeXamlLoader.Load(@"
+<Button xmlns='https://github.com/avaloniaui'>
+    <Design.PreviewWith>
+        <Template>
+            <Border>
+                <Button />
+            </Border>
+        </Template>
+    </Design.PreviewWith>
+</Button>", designMode: true);
+            var preview = Design.CreatePreviewWithControl(obj);
+            var previewBorder = Assert.IsType<Border>(preview);
+            Assert.IsType<Button>(previewBorder.Child);
+        }
+    }
+
+    [Fact]
+    public void Design_Mode_PreviewWith_Works_With_Style()
+    {
+        using (UnitTestApplication.Start(TestServices.MockWindowingPlatform))
+        {
+            var obj = (Style)AvaloniaRuntimeXamlLoader.Load(@"
+<Style xmlns='https://github.com/avaloniaui'
+       xmlns:x='http://schemas.microsoft.com/winfx/2006/xaml'
+       Selector='Border.preview-border' >
+    <Design.PreviewWith>
+        <Border Classes='preview-border' />
+    </Design.PreviewWith>
+    <Setter Property='Background' Value='Red'/>
+</Style>", designMode: true);
+            var preview = Design.CreatePreviewWithControl(obj);
+            var previewBorder = Assert.IsType<Border>(preview);
+            previewBorder.ApplyStyling();
+            Assert.Equal(Colors.Red, (previewBorder.Background as ISolidColorBrush)?.Color);
+        }
+    }
+
+    [Fact]
+    public void Design_Mode_PreviewWith_Works_With_ResourceDictionary()
+    {
+        using (UnitTestApplication.Start(TestServices.MockWindowingPlatform))
+        {
+            var obj = (ResourceDictionary)AvaloniaRuntimeXamlLoader.Load(@"
+<ResourceDictionary xmlns='https://github.com/avaloniaui'
+                    xmlns:x='http://schemas.microsoft.com/winfx/2006/xaml'>
+    <Design.PreviewWith>
+        <Border Background='{DynamicResource PreviewBackground}' />
+    </Design.PreviewWith>
+    <SolidColorBrush x:Key='PreviewBackground' Color='Red'/>
+</ResourceDictionary>", designMode: true);
+            var preview = Design.CreatePreviewWithControl(obj);
+            var previewBorder = Assert.IsType<Border>(preview);
+            Assert.Equal(Colors.Red, (previewBorder.Background as ISolidColorBrush)?.Color);
+        }
+    }
+
+    [Fact]
+    public void Design_Mode_PreviewWith_Works_With_IDataTemplate()
+    {
+        using (UnitTestApplication.Start(TestServices.MockWindowingPlatform))
+        {
+            var obj = (DataTemplate)AvaloniaRuntimeXamlLoader.Load(@"
+<DataTemplate xmlns='https://github.com/avaloniaui'
+              xmlns:x='http://schemas.microsoft.com/winfx/2006/xaml'
+              x:DataType='SolidColorBrush'>
+    <Design.PreviewWith>
+        <ContentControl>
+            <ContentControl.Content>
+                <SolidColorBrush Color='Red'/>
+            </ContentControl.Content>
+        </ContentControl>
+    </Design.PreviewWith>
+    <Border Background='{Binding}' />
+</DataTemplate>", designMode: true);
+            var preview = Design.CreatePreviewWithControl(obj);
+            var previewContentControl = Assert.IsType<ContentControl>(preview);
+            previewContentControl.ApplyTemplate();
+            previewContentControl.Presenter!.UpdateChild();
+            var border = previewContentControl.FindDescendantOfType<Border>();
+            Assert.NotNull(border);
+            Assert.Equal(Colors.Red, (border.Background as ISolidColorBrush)?.Color);
+        }
+    }
+
+    [Fact]
+    public void Design_Mode_Properties_Should_Be_Ignored_At_Runtime_And_Set_In_Design_Mode()
+    {
+        using (UnitTestApplication.Start(TestServices.MockWindowingPlatform))
+        {
+            foreach (var designMode in new[] { true, false })
+            {
+                var obj = (Window)AvaloniaRuntimeXamlLoader.Load(@"
+<Window xmlns='https://github.com/avaloniaui' 
+        xmlns:d='http://schemas.microsoft.com/expression/blend/2008'
+        xmlns:mc='http://schemas.openxmlformats.org/markup-compatibility/2006'
+        mc:Ignorable='d'
+        d:DataContext='data-context'
+        d:DesignWidth='123'
+        d:DesignHeight='321'>
+</Window>", designMode: designMode);
+                var context = Design.GetDataContext(obj);
+                var width = Design.GetWidth(obj);
+                var height = Design.GetHeight(obj);
+                if (designMode)
+                {
+                    Assert.Equal("data-context", context);
+                    Assert.Equal(123, width);
+                    Assert.Equal(321, height);
+                }
+                else
+                {
+                    Assert.False(obj.IsSet(Design.DataContextProperty));
+                    Assert.False(obj.IsSet(Design.WidthProperty));
+                    Assert.False(obj.IsSet(Design.HeightProperty));
+                }
+            }
+        }
+    }
+
+    // https://github.com/AvaloniaUI/Avalonia/issues/2570
+    [Fact]
+    public void Design_Mode_Throws_On_Invalid_Static_Property_Reference()
+    {
+        SomeStaticProperty = "123";
+        var ex = Assert.ThrowsAny<Exception>(() => AvaloniaRuntimeXamlLoader
+            .Load(@"
+<UserControl 
+    xmlns='https://github.com/avaloniaui'
+    xmlns:d='http://schemas.microsoft.com/expression/blend/2008'
+    xmlns:tests='using:Avalonia.Markup.Xaml.UnitTests.Xaml'
+    d:DataContext='{x:Static tests:DesignModeTests.SomeStaticPropery}'
+    xmlns:x='http://schemas.microsoft.com/winfx/2006/xaml'/>", typeof(XamlIlTests).Assembly,
+                designMode: true));
+        Assert.Contains("Unable to resolve ", ex.Message);
+        Assert.Contains(" as static field, property, constant or enum value", ex.Message);
+    }
+
+    [Fact]
+    public void Design_Mode_DataContext_Should_Be_Set()
+    {
+        SomeStaticProperty = "123";
+
+        var loaded = (UserControl)AvaloniaRuntimeXamlLoader
+            .Load(@"
+<UserControl 
+    xmlns='https://github.com/avaloniaui'
+    xmlns:d='http://schemas.microsoft.com/expression/blend/2008'
+    xmlns:tests='using:Avalonia.Markup.Xaml.UnitTests.Xaml'
+    d:DataContext='{x:Static tests:DesignModeTests.SomeStaticProperty}'
+    xmlns:x='http://schemas.microsoft.com/winfx/2006/xaml'/>", typeof(XamlIlTests).Assembly,
+                designMode: true);
+        Assert.Equal(Design.GetDataContext(loaded), SomeStaticProperty);
+    }
+}
diff --git a/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/XamlIlTests.cs b/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/XamlIlTests.cs
index afb09c2838..cb42fe2a62 100644
--- a/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/XamlIlTests.cs
+++ b/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/XamlIlTests.cs
@@ -7,11 +7,8 @@ using System.Runtime.CompilerServices;
 using Avalonia.Controls;
 using Avalonia.Data.Converters;
 using Avalonia.Data.Core;
-using Avalonia.Input;
-using Avalonia.Interactivity;
 using Avalonia.Markup.Xaml.UnitTests.Xaml;
 using Avalonia.Media;
-using Avalonia.Styling;
 using Avalonia.Threading;
 using Avalonia.UnitTests;
 using Avalonia.VisualTree;
@@ -151,57 +148,6 @@ namespace Avalonia.Markup.Xaml.UnitTests
             
         }
 
-        static void AssertThrows(Action callback, Func<Exception, bool> check)
-        {
-            try
-            {
-                callback();
-            }
-            catch (Exception e) when (check(e))
-            {
-                return;
-            }
-
-            throw new Exception("Expected exception was not thrown");
-        }
-        
-        public static object SomeStaticProperty { get; set; }
-
-        [Fact]
-        public void Bug2570()
-        {
-            SomeStaticProperty = "123";
-            AssertThrows(() => AvaloniaRuntimeXamlLoader
-                    .Load(@"
-<UserControl 
-    xmlns='https://github.com/avaloniaui'
-    xmlns:d='http://schemas.microsoft.com/expression/blend/2008'
-    xmlns:tests='clr-namespace:Avalonia.Markup.Xaml.UnitTests'
-    d:DataContext='{x:Static tests:XamlIlTests.SomeStaticPropery}'
-    xmlns:x='http://schemas.microsoft.com/winfx/2006/xaml'/>", typeof(XamlIlTests).Assembly,
-                        designMode: true),
-                e => e.Message.Contains("Unable to resolve ")
-                     && e.Message.Contains(" as static field, property, constant or enum value"));
-
-        }
-        
-        [Fact]
-        public void Design_Mode_DataContext_Should_Be_Set()
-        {
-            SomeStaticProperty = "123";
-            
-            var loaded = (UserControl)AvaloniaRuntimeXamlLoader
-                .Load(@"
-<UserControl 
-    xmlns='https://github.com/avaloniaui'
-    xmlns:d='http://schemas.microsoft.com/expression/blend/2008'
-    xmlns:tests='clr-namespace:Avalonia.Markup.Xaml.UnitTests'
-    d:DataContext='{x:Static tests:XamlIlTests.SomeStaticProperty}'
-    xmlns:x='http://schemas.microsoft.com/winfx/2006/xaml'/>", typeof(XamlIlTests).Assembly,
-                    designMode: true);
-            Assert.Equal(Design.GetDataContext(loaded), SomeStaticProperty);
-        }
-        
         [Fact]
         public void Attached_Properties_From_Static_Types_Should_Work_In_Style_Setters_Bug_2561()
         {