diff --git a/src/Avalonia.Base/Metadata/InheritDataTypeFromItemsAttribute.cs b/src/Avalonia.Base/Metadata/InheritDataTypeFromItemsAttribute.cs
index fac8cd8737..e9bd6ab89f 100644
--- a/src/Avalonia.Base/Metadata/InheritDataTypeFromItemsAttribute.cs
+++ b/src/Avalonia.Base/Metadata/InheritDataTypeFromItemsAttribute.cs
@@ -9,7 +9,7 @@ namespace Avalonia.Metadata;
 /// A typical usage example is a ListBox control, where <see cref="InheritDataTypeFromItemsAttribute"/> is defined on the ItemTemplate property,
 /// allowing the template to inherit the data type from the Items collection binding. 
 /// </remarks>
-[AttributeUsage(AttributeTargets.Property, AllowMultiple = false, Inherited = true)]
+[AttributeUsage(AttributeTargets.Property, AllowMultiple = true, Inherited = true)]
 public sealed class InheritDataTypeFromItemsAttribute : Attribute
 {
     /// <summary>
diff --git a/src/Avalonia.Controls/ItemsControl.cs b/src/Avalonia.Controls/ItemsControl.cs
index 56ba9c7183..4914a833de 100644
--- a/src/Avalonia.Controls/ItemsControl.cs
+++ b/src/Avalonia.Controls/ItemsControl.cs
@@ -95,6 +95,7 @@ namespace Avalonia.Controls
         /// </summary>
         [AssignBinding]
         [InheritDataTypeFromItems(nameof(ItemsSource))]
+        [InheritDataTypeFromItems(nameof(Items))]
         public IBinding? DisplayMemberBinding
         {
             get => GetValue(DisplayMemberBindingProperty);
@@ -218,6 +219,7 @@ namespace Avalonia.Controls
         /// Gets or sets the data template used to display the items in the control.
         /// </summary>
         [InheritDataTypeFromItems(nameof(ItemsSource))]
+        [InheritDataTypeFromItems(nameof(Items))]
         public IDataTemplate? ItemTemplate
         {
             get => GetValue(ItemTemplateProperty);
diff --git a/src/Avalonia.Controls/Primitives/SelectingItemsControl.cs b/src/Avalonia.Controls/Primitives/SelectingItemsControl.cs
index 7716e32e26..a31472fab4 100644
--- a/src/Avalonia.Controls/Primitives/SelectingItemsControl.cs
+++ b/src/Avalonia.Controls/Primitives/SelectingItemsControl.cs
@@ -235,6 +235,7 @@ namespace Avalonia.Controls.Primitives
         /// </summary>
         [AssignBinding]
         [InheritDataTypeFromItems(nameof(ItemsSource))]
+        [InheritDataTypeFromItems(nameof(Items))]
         public IBinding? SelectedValueBinding
         {
             get => GetValue(SelectedValueBindingProperty);
diff --git a/src/Markup/Avalonia.Markup.Xaml.Loader/CompilerExtensions/Transformers/AvaloniaXamlIlDataContextTypeTransformer.cs b/src/Markup/Avalonia.Markup.Xaml.Loader/CompilerExtensions/Transformers/AvaloniaXamlIlDataContextTypeTransformer.cs
index a24d4eb6e9..681d2a38d4 100644
--- a/src/Markup/Avalonia.Markup.Xaml.Loader/CompilerExtensions/Transformers/AvaloniaXamlIlDataContextTypeTransformer.cs
+++ b/src/Markup/Avalonia.Markup.Xaml.Loader/CompilerExtensions/Transformers/AvaloniaXamlIlDataContextTypeTransformer.cs
@@ -73,27 +73,32 @@ namespace Avalonia.Markup.Xaml.XamlIl.CompilerExtensions.Transformers
                     // Infer data type from collection binding on a control that displays items.
                     var property = context.ParentNodes().OfType<XamlPropertyAssignmentNode>().FirstOrDefault();
                     var attributeType = context.GetAvaloniaTypes().InheritDataTypeFromItemsAttribute;
-                    var attribute = property?.Property?.GetClrProperty().CustomAttributes
-                        .FirstOrDefault(a => a.Type == attributeType);
-    
-                    if (attribute is not null)
+                    var attributes = property?.Property?.GetClrProperty().CustomAttributes
+                        .Where(a => a.Type == attributeType).ToList();
+
+                    if (attributes?.Count > 0)
                     {
-                        var propertyName = (string)attribute.Parameters.First();
-                        XamlAstConstructableObjectNode parentObject;
-                        if (attribute.Properties.TryGetValue("AncestorType", out var type)
-                            && type is IXamlType xamlType)
-                        {
-                            parentObject = context.ParentNodes().OfType<XamlAstConstructableObjectNode>()
-                                .FirstOrDefault(n => n.Type.GetClrType().FullName == xamlType.FullName);
-                        }
-                        else
+                        foreach (var attribute in attributes)
                         {
-                            parentObject = context.ParentNodes().OfType<XamlAstConstructableObjectNode>().FirstOrDefault();
-                        }
-                            
-                        if (parentObject != null)
-                        {
-                            inferredDataContextTypeNode = InferDataContextOfPresentedItem(context, on, parentObject, propertyName);
+                            var propertyName = (string)attribute.Parameters.First();
+                            XamlAstConstructableObjectNode parentObject;
+                            if (attribute.Properties.TryGetValue("AncestorType", out var type)
+                                && type is IXamlType xamlType)
+                            {
+                                parentObject = context.ParentNodes().OfType<XamlAstConstructableObjectNode>()
+                                    .FirstOrDefault(n => n.Type.GetClrType().FullName == xamlType.FullName);
+                            }
+                            else
+                            {
+                                parentObject = context.ParentNodes().OfType<XamlAstConstructableObjectNode>().FirstOrDefault();
+                            }
+
+                            if (parentObject != null)
+                            {
+                                inferredDataContextTypeNode = InferDataContextOfPresentedItem(context, on, parentObject, propertyName);
+                                if (inferredDataContextTypeNode != null)
+                                    break;
+                            }
                         }
                     }