diff --git a/src/libraries/System.Text.Json/src/System.Text.Json.csproj b/src/libraries/System.Text.Json/src/System.Text.Json.csproj
index e17ce01c77035..8cd779f5a0218 100644
--- a/src/libraries/System.Text.Json/src/System.Text.Json.csproj
+++ b/src/libraries/System.Text.Json/src/System.Text.Json.csproj
@@ -36,6 +36,7 @@ The System.Text.Json library is built-in as part of the shared framework in .NET
     <Compile Include="..\Common\JsonSourceGenerationMode.cs" Link="Common\System\Text\Json\Serialization\JsonSourceGenerationMode.cs" />
     <Compile Include="..\Common\JsonSourceGenerationOptionsAttribute.cs" Link="Common\System\Text\Json\Serialization\JsonSourceGenerationOptionsAttribute.cs" />
     <Compile Include="..\Common\ReflectionExtensions.cs" Link="Common\System\Text\Json\Serialization\ReflectionExtensions.cs" />
+    <Compile Include="System\Text\Json\AppContextSwitchHelper.cs" />
     <Compile Include="System\Text\Json\BitStack.cs" />
     <Compile Include="System\Text\Json\Document\JsonDocument.cs" />
     <Compile Include="System\Text\Json\Document\JsonDocument.DbRow.cs" />
diff --git a/src/libraries/System.Text.Json/src/System/Text/Json/AppContextSwitchHelper.cs b/src/libraries/System.Text.Json/src/System/Text/Json/AppContextSwitchHelper.cs
new file mode 100644
index 0000000000000..9c028f0216517
--- /dev/null
+++ b/src/libraries/System.Text.Json/src/System/Text/Json/AppContextSwitchHelper.cs
@@ -0,0 +1,16 @@
+// Licensed to the .NET Foundation under one or more agreements.
+// The .NET Foundation licenses this file to you under the MIT license.
+
+namespace System.Text.Json
+{
+    internal static class AppContextSwitchHelper
+    {
+        public static bool IsSourceGenReflectionFallbackEnabled => s_isSourceGenReflectionFallbackEnabled;
+
+        private static readonly bool s_isSourceGenReflectionFallbackEnabled =
+            AppContext.TryGetSwitch(
+                switchName: "System.Text.Json.Serialization.EnableSourceGenReflectionFallback",
+                isEnabled: out bool value)
+            ? value : false;
+    }
+}
diff --git a/src/libraries/System.Text.Json/src/System/Text/Json/Serialization/JsonSerializerOptions.cs b/src/libraries/System.Text.Json/src/System/Text/Json/Serialization/JsonSerializerOptions.cs
index 596a9c37bae48..fa543671792fb 100644
--- a/src/libraries/System.Text.Json/src/System/Text/Json/Serialization/JsonSerializerOptions.cs
+++ b/src/libraries/System.Text.Json/src/System/Text/Json/Serialization/JsonSerializerOptions.cs
@@ -628,7 +628,20 @@ internal void InitializeForReflectionSerializer()
             // Even if a resolver has already been specified, we need to root
             // the default resolver to gain access to the default converters.
             DefaultJsonTypeInfoResolver defaultResolver = DefaultJsonTypeInfoResolver.RootDefaultInstance();
-            _typeInfoResolver ??= defaultResolver;
+
+            switch (_typeInfoResolver)
+            {
+                case null:
+                    // Use the default reflection-based resolver if no resolver has been specified.
+                    _typeInfoResolver = defaultResolver;
+                    break;
+
+                case JsonSerializerContext ctx when AppContextSwitchHelper.IsSourceGenReflectionFallbackEnabled:
+                    // .NET 6 compatibility mode: enable fallback to reflection metadata for JsonSerializerContext
+                    _effectiveJsonTypeInfoResolver = JsonTypeInfoResolver.Combine(ctx, defaultResolver);
+                    break;
+            }
+
             IsImmutable = true;
             _isInitializedForReflectionSerializer = true;
         }
@@ -636,6 +649,9 @@ internal void InitializeForReflectionSerializer()
         internal bool IsInitializedForReflectionSerializer => _isInitializedForReflectionSerializer;
         private volatile bool _isInitializedForReflectionSerializer;
 
+        // Only populated in .NET 6 compatibility mode encoding reflection fallback in source gen
+        private IJsonTypeInfoResolver? _effectiveJsonTypeInfoResolver;
+
         internal void InitializeForMetadataGeneration()
         {
             if (_typeInfoResolver is null)
@@ -648,7 +664,7 @@ internal void InitializeForMetadataGeneration()
 
         private JsonTypeInfo? GetTypeInfoNoCaching(Type type)
         {
-            JsonTypeInfo? info = _typeInfoResolver?.GetTypeInfo(type, this);
+            JsonTypeInfo? info = (_effectiveJsonTypeInfoResolver ?? _typeInfoResolver)?.GetTypeInfo(type, this);
 
             if (info != null)
             {
diff --git a/src/libraries/System.Text.Json/tests/System.Text.Json.Tests/Serialization/OptionsTests.cs b/src/libraries/System.Text.Json/tests/System.Text.Json.Tests/Serialization/OptionsTests.cs
index a91467a9943a3..05cd443bccf5a 100644
--- a/src/libraries/System.Text.Json/tests/System.Text.Json.Tests/Serialization/OptionsTests.cs
+++ b/src/libraries/System.Text.Json/tests/System.Text.Json.Tests/Serialization/OptionsTests.cs
@@ -437,9 +437,18 @@ public static void Options_JsonSerializerContext_DoesNotFallbackToReflection()
         }
 
         [SkipOnTargetFramework(TargetFrameworkMonikers.NetFramework)]
-        [ConditionalFact(typeof(RemoteExecutor), nameof(RemoteExecutor.IsSupported))]
-        public static void Options_JsonSerializerContext_GetConverter_DoesNotFallBackToReflectionConverter()
+        [ConditionalTheory(typeof(RemoteExecutor), nameof(RemoteExecutor.IsSupported))]
+        [InlineData(false)]
+        [InlineData(true)]
+        public static void Options_JsonSerializerContext_GetConverter_DoesNotFallBackToReflectionConverter(bool isCompatibilitySwitchExplicitlyDisabled)
         {
+            var options = new RemoteInvokeOptions();
+
+            if (isCompatibilitySwitchExplicitlyDisabled)
+            {
+                options.RuntimeConfigurationOptions.Add("System.Text.Json.Serialization.EnableSourceGenReflectionFallback", false);
+            }
+
             RemoteExecutor.Invoke(static () =>
             {
                 JsonContext context = JsonContext.Default;
@@ -460,7 +469,40 @@ public static void Options_JsonSerializerContext_GetConverter_DoesNotFallBackToR
                 Assert.Throws<NotSupportedException>(() => context.Options.GetConverter(typeof(MyClass)));
                 Assert.Throws<NotSupportedException>(() => JsonSerializer.Serialize(unsupportedValue, context.Options));
 
-            }).Dispose();
+            }, options).Dispose();
+        }
+
+        [SkipOnTargetFramework(TargetFrameworkMonikers.NetFramework)]
+        [ConditionalFact(typeof(RemoteExecutor), nameof(RemoteExecutor.IsSupported))]
+        public static void Options_JsonSerializerContext_Net6CompatibilitySwitch_FallsBackToReflectionResolver()
+        {
+            var options = new RemoteInvokeOptions
+            {
+                RuntimeConfigurationOptions =
+                {
+                    ["System.Text.Json.Serialization.EnableSourceGenReflectionFallback"] = true
+                }
+            };
+            
+            RemoteExecutor.Invoke(static () =>
+            {
+                var unsupportedValue = new MyClass { Value = "value" };
+
+                // JsonSerializerContext does not return metadata for the type
+                Assert.Null(JsonContext.Default.GetTypeInfo(typeof(MyClass)));
+
+                // Serialization fails using the JsonSerializerContext overload
+                Assert.Throws<InvalidOperationException>(() => JsonSerializer.Serialize(unsupportedValue, unsupportedValue.GetType(), JsonContext.Default));
+
+                // Serialization uses reflection fallback using the JsonSerializerOptions overload
+                string json = JsonSerializer.Serialize(unsupportedValue, JsonContext.Default.Options);
+                JsonTestHelper.AssertJsonEqual("""{"Value":"value", "Thing":null}""", json);
+
+                // A converter can be resolved when looking up JsonSerializerOptions
+                JsonConverter converter = JsonContext.Default.Options.GetConverter(typeof(MyClass));
+                Assert.IsAssignableFrom<JsonConverter<MyClass>>(converter);
+
+            }, options).Dispose();
         }
 
         [Fact]