diff --git a/src/Http/Http.Extensions/test/RequestDelegateFactoryTests.cs b/src/Http/Http.Extensions/test/RequestDelegateFactoryTests.cs
index d37206d6b411..0de35134714b 100644
--- a/src/Http/Http.Extensions/test/RequestDelegateFactoryTests.cs
+++ b/src/Http/Http.Extensions/test/RequestDelegateFactoryTests.cs
@@ -29,6 +29,7 @@
 using Microsoft.AspNetCore.Http.Metadata;
 using Microsoft.AspNetCore.Routing.Patterns;
 using Microsoft.AspNetCore.Testing;
+using Microsoft.DotNet.RemoteExecutor;
 using Microsoft.Extensions.DependencyInjection;
 using Microsoft.Extensions.Internal;
 using Microsoft.Extensions.Logging;
@@ -2903,6 +2904,44 @@ static void TestAction([AsParameters] ParameterListMixedRequiredStringsFromDiffe
     }
 #nullable enable
 
+    [ConditionalFact]
+    [RemoteExecutionSupported]
+    public void RequestDelegateFactory_WhenJsonIsReflectionEnabledByDefaultFalse()
+    {
+        var options = new RemoteInvokeOptions();
+        options.RuntimeConfigurationOptions.Add("System.Text.Json.JsonSerializer.IsReflectionEnabledByDefault", false.ToString());
+
+        using var remoteHandle = RemoteExecutor.Invoke(static () =>
+        {
+            // Arrange
+            var @delegate = (string task) => new Todo();
+
+            // IsReflectionEnabledByDefault defaults to `false` when `PublishTrimmed=true`. For these scenarios, we
+            // expect users to configure JSON source generation as instructed in the `NotSupportedException` message.
+            var exception = Assert.Throws<NotSupportedException>(() => RequestDelegateFactory.Create(@delegate));
+            Assert.Contains("Microsoft.AspNetCore.Routing.Internal.RequestDelegateFactoryTests+Todo", exception.Message);
+            Assert.Contains("JsonSerializableAttribute", exception.Message);
+        }, options);
+    }
+
+    [ConditionalFact]
+    [RemoteExecutionSupported]
+    public void RequestDelegateFactory_WhenJsonIsReflectionEnabledByDefaultTrue()
+    {
+        var options = new RemoteInvokeOptions();
+        options.RuntimeConfigurationOptions.Add("System.Text.Json.JsonSerializer.IsReflectionEnabledByDefault", true.ToString());
+
+        using var remoteHandle = RemoteExecutor.Invoke(static () =>
+        {
+            // Arrange
+            var @delegate = (string task) => new Todo();
+
+            // Assert
+            var exception = Record.Exception(() => RequestDelegateFactory.Create(@delegate));
+            Assert.Null(exception);
+        }, options);
+    }
+
     private DefaultHttpContext CreateHttpContext()
     {
         var responseFeature = new TestHttpResponseFeature();
diff --git a/src/Mvc/Mvc.Core/src/Formatters/SystemTextJsonOutputFormatter.cs b/src/Mvc/Mvc.Core/src/Formatters/SystemTextJsonOutputFormatter.cs
index 273b11d6f65d..35000cb21ae2 100644
--- a/src/Mvc/Mvc.Core/src/Formatters/SystemTextJsonOutputFormatter.cs
+++ b/src/Mvc/Mvc.Core/src/Formatters/SystemTextJsonOutputFormatter.cs
@@ -23,6 +23,8 @@ public SystemTextJsonOutputFormatter(JsonSerializerOptions jsonSerializerOptions
     {
         SerializerOptions = jsonSerializerOptions;
 
+        // Use JsonTypeInfoResolver.Combine() to produce an empty TypeInfoResolver
+        jsonSerializerOptions.TypeInfoResolver ??= JsonTypeInfoResolver.Combine();
         jsonSerializerOptions.MakeReadOnly();
 
         SupportedEncodings.Add(Encoding.UTF8);
diff --git a/src/Mvc/Mvc.Core/test/Formatters/SystemTextJsonOutputFormatterTest.cs b/src/Mvc/Mvc.Core/test/Formatters/SystemTextJsonOutputFormatterTest.cs
index 203f03590831..d16ce19fb9da 100644
--- a/src/Mvc/Mvc.Core/test/Formatters/SystemTextJsonOutputFormatterTest.cs
+++ b/src/Mvc/Mvc.Core/test/Formatters/SystemTextJsonOutputFormatterTest.cs
@@ -6,6 +6,8 @@
 using System.Text.Json;
 using System.Text.Json.Serialization;
 using System.Text.Json.Serialization.Metadata;
+using Microsoft.AspNetCore.Testing;
+using Microsoft.DotNet.RemoteExecutor;
 using Microsoft.Extensions.Primitives;
 using Microsoft.Net.Http.Headers;
 
@@ -254,13 +256,39 @@ private static async IAsyncEnumerable<JsonPerson> GetPeopleAsync()
     }
 
     [Fact]
-    public void WriteResponseBodyAsync_Throws_WhenTypeResolverIsNull()
+    public void WriteResponseBodyAsync_Works_WhenTypeResolverIsNull()
     {
         // Arrange
         var jsonOptions = new JsonOptions();
         jsonOptions.JsonSerializerOptions.TypeInfoResolver = null;
 
-        Assert.Throws<InvalidOperationException>(() => SystemTextJsonOutputFormatter.CreateFormatter(jsonOptions));
+        var stjOutputFormatter = SystemTextJsonOutputFormatter.CreateFormatter(jsonOptions);
+        Assert.IsAssignableFrom<IJsonTypeInfoResolver>(stjOutputFormatter.SerializerOptions.TypeInfoResolver);
+    }
+
+    [ConditionalTheory]
+    [RemoteExecutionSupported]
+    [InlineData(false)]
+    [InlineData(true)]
+    public void STJOutputFormatter_UsesEmptyResolver_WhenJsonIsReflectionEnabledByDefaultFalse(bool isReflectionEnabledByDefault)
+    {
+        var options = new RemoteInvokeOptions();
+        options.RuntimeConfigurationOptions.Add("System.Text.Json.JsonSerializer.IsReflectionEnabledByDefault", isReflectionEnabledByDefault.ToString());
+
+        using var remoteHandle = RemoteExecutor.Invoke(static () =>
+        {
+            // Arrange
+            var jsonOptions = new JsonOptions();
+
+            // Assert
+            var stjOutputFormatter = SystemTextJsonOutputFormatter.CreateFormatter(jsonOptions);
+            Assert.IsAssignableFrom<IJsonTypeInfoResolver>(stjOutputFormatter.SerializerOptions.TypeInfoResolver);
+            // Use default resolver if reflection is enabled instead of empty one
+            if (JsonSerializer.IsReflectionEnabledByDefault)
+            {
+                Assert.IsType<DefaultJsonTypeInfoResolver>(stjOutputFormatter.SerializerOptions.TypeInfoResolver);
+            }
+        }, options);
     }
 
     private class Person
diff --git a/src/Shared/Json/JsonSerializerExtensions.cs b/src/Shared/Json/JsonSerializerExtensions.cs
index 7068649a63f5..36f823efbd56 100644
--- a/src/Shared/Json/JsonSerializerExtensions.cs
+++ b/src/Shared/Json/JsonSerializerExtensions.cs
@@ -18,6 +18,8 @@ public static bool ShouldUseWith(this JsonTypeInfo jsonTypeInfo, [NotNullWhen(fa
 
     public static JsonTypeInfo GetReadOnlyTypeInfo(this JsonSerializerOptions options, Type type)
     {
+        // Use JsonTypeInfoResolver.Combine() to produce an empty TypeInfoResolver
+        options.TypeInfoResolver ??= JsonTypeInfoResolver.Combine();
         options.MakeReadOnly();
         return options.GetTypeInfo(type);
     }