diff --git a/src/libraries/System.Text.Json/src/System/Text/Json/Serialization/Metadata/DefaultJsonTypeInfoResolver.Helpers.cs b/src/libraries/System.Text.Json/src/System/Text/Json/Serialization/Metadata/DefaultJsonTypeInfoResolver.Helpers.cs
index a6b71ea822077..c5d44694c7193 100644
--- a/src/libraries/System.Text.Json/src/System/Text/Json/Serialization/Metadata/DefaultJsonTypeInfoResolver.Helpers.cs
+++ b/src/libraries/System.Text.Json/src/System/Text/Json/Serialization/Metadata/DefaultJsonTypeInfoResolver.Helpers.cs
@@ -13,6 +13,9 @@ namespace System.Text.Json.Serialization.Metadata
 {
     public partial class DefaultJsonTypeInfoResolver
     {
+        private static readonly bool s_isNullabilityInfoContextSupported =
+            AppContext.TryGetSwitch("System.Reflection.NullabilityInfoContext.IsSupported", out bool isSupported) ? isSupported : true;
+
         internal static MemberAccessor MemberAccessor
         {
             [RequiresUnreferencedCode(JsonSerializer.SerializationRequiresDynamicCodeMessage)]
@@ -71,7 +74,10 @@ private static JsonTypeInfo CreateTypeInfoCore(Type type, JsonConverter converte
 
             if (typeInfo.Kind is JsonTypeInfoKind.Object)
             {
-                NullabilityInfoContext nullabilityCtx = new();
+                // If the System.Reflection.NullabilityInfoContext.IsSupported feature switch has been disabled,
+                // we want to avoid resolving nullability information for properties and parameters unless the
+                // user has explicitly opted into nullability enforcement in which case an exception will be surfaced.
+                NullabilityInfoContext? nullabilityCtx = s_isNullabilityInfoContextSupported || options.RespectNullableAnnotations ? new() : null;
 
                 if (converter.ConstructorIsParameterized)
                 {
@@ -91,7 +97,7 @@ private static JsonTypeInfo CreateTypeInfoCore(Type type, JsonConverter converte
 
         [RequiresUnreferencedCode(JsonSerializer.SerializationUnreferencedCodeMessage)]
         [RequiresDynamicCode(JsonSerializer.SerializationRequiresDynamicCodeMessage)]
-        private static void PopulateProperties(JsonTypeInfo typeInfo, NullabilityInfoContext nullabilityCtx)
+        private static void PopulateProperties(JsonTypeInfo typeInfo, NullabilityInfoContext? nullabilityCtx)
         {
             Debug.Assert(!typeInfo.IsReadOnly);
             Debug.Assert(typeInfo.Kind is JsonTypeInfoKind.Object);
@@ -158,7 +164,7 @@ private static void PopulateProperties(JsonTypeInfo typeInfo, NullabilityInfoCon
         private static void AddMembersDeclaredBySuperType(
             JsonTypeInfo typeInfo,
             Type currentType,
-            NullabilityInfoContext nullabilityCtx,
+            NullabilityInfoContext? nullabilityCtx,
             bool constructorHasSetsRequiredMembersAttribute,
             ref JsonTypeInfo.PropertyHierarchyResolutionState state)
         {
@@ -219,7 +225,7 @@ private static void AddMember(
             JsonTypeInfo typeInfo,
             Type typeToConvert,
             MemberInfo memberInfo,
-            NullabilityInfoContext nullabilityCtx,
+            NullabilityInfoContext? nullabilityCtx,
             bool shouldCheckForRequiredKeyword,
             bool hasJsonIncludeAttribute,
             ref JsonTypeInfo.PropertyHierarchyResolutionState state)
@@ -241,7 +247,7 @@ private static void AddMember(
             JsonTypeInfo typeInfo,
             Type typeToConvert,
             MemberInfo memberInfo,
-            NullabilityInfoContext nullabilityCtx,
+            NullabilityInfoContext? nullabilityCtx,
             JsonSerializerOptions options,
             bool shouldCheckForRequiredKeyword,
             bool hasJsonIncludeAttribute)
@@ -301,7 +307,7 @@ private static bool PropertyIsOverriddenAndIgnored(PropertyInfo propertyInfo, Di
 
         [RequiresUnreferencedCode(JsonSerializer.SerializationUnreferencedCodeMessage)]
         [RequiresDynamicCode(JsonSerializer.SerializationRequiresDynamicCodeMessage)]
-        private static void PopulateParameterInfoValues(JsonTypeInfo typeInfo, NullabilityInfoContext nullabilityCtx)
+        private static void PopulateParameterInfoValues(JsonTypeInfo typeInfo, NullabilityInfoContext? nullabilityCtx)
         {
             Debug.Assert(typeInfo.Converter.ConstructorInfo != null);
             ParameterInfo[] parameters = typeInfo.Converter.ConstructorInfo.GetParameters();
@@ -326,9 +332,7 @@ private static void PopulateParameterInfoValues(JsonTypeInfo typeInfo, Nullabili
                     Position = reflectionInfo.Position,
                     HasDefaultValue = reflectionInfo.HasDefaultValue,
                     DefaultValue = reflectionInfo.GetDefaultValue(),
-                    IsNullable =
-                        reflectionInfo.ParameterType.IsNullableType() &&
-                        DetermineParameterNullability(reflectionInfo, nullabilityCtx) is not NullabilityState.NotNull,
+                    IsNullable = DetermineParameterNullability(reflectionInfo, nullabilityCtx) is not NullabilityState.NotNull,
                 };
 
                 jsonParameters[i] = jsonInfo;
@@ -344,7 +348,7 @@ private static void PopulatePropertyInfo(
             MemberInfo memberInfo,
             JsonConverter? customConverter,
             JsonIgnoreCondition? ignoreCondition,
-            NullabilityInfoContext nullabilityCtx,
+            NullabilityInfoContext? nullabilityCtx,
             bool shouldCheckForRequiredKeyword,
             bool hasJsonIncludeAttribute)
         {
@@ -487,9 +491,9 @@ internal static void DeterminePropertyAccessors<T>(JsonPropertyInfo<T> jsonPrope
 
         [RequiresUnreferencedCode(JsonSerializer.SerializationUnreferencedCodeMessage)]
         [RequiresDynamicCode(JsonSerializer.SerializationRequiresDynamicCodeMessage)]
-        private static void DeterminePropertyNullability(JsonPropertyInfo propertyInfo, MemberInfo memberInfo, NullabilityInfoContext nullabilityCtx)
+        private static void DeterminePropertyNullability(JsonPropertyInfo propertyInfo, MemberInfo memberInfo, NullabilityInfoContext? nullabilityCtx)
         {
-            if (!propertyInfo.PropertyTypeCanBeNull)
+            if (!propertyInfo.PropertyTypeCanBeNull || nullabilityCtx is null)
             {
                 return;
             }
@@ -511,8 +515,17 @@ private static void DeterminePropertyNullability(JsonPropertyInfo propertyInfo,
 
         [RequiresUnreferencedCode(JsonSerializer.SerializationUnreferencedCodeMessage)]
         [RequiresDynamicCode(JsonSerializer.SerializationRequiresDynamicCodeMessage)]
-        private static NullabilityState DetermineParameterNullability(ParameterInfo parameterInfo, NullabilityInfoContext nullabilityCtx)
+        private static NullabilityState DetermineParameterNullability(ParameterInfo parameterInfo, NullabilityInfoContext? nullabilityCtx)
         {
+            if (!parameterInfo.ParameterType.IsNullableType())
+            {
+                return NullabilityState.NotNull;
+            }
+
+            if (nullabilityCtx is null)
+            {
+                return NullabilityState.Unknown;
+            }
 #if NET8_0
             // Workaround for https://github.com/dotnet/runtime/issues/92487
             // The fix has been incorporated into .NET 9 (and the polyfilled implementations in netfx).
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 3ada5243181d7..f5ef9964d8f1c 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
@@ -960,6 +960,60 @@ public static void Options_RespectNullableAnnotationsDefault_FeatureSwitch(bool?
             }, arg, options).Dispose();
         }
 
+        [SkipOnTargetFramework(TargetFrameworkMonikers.NetFramework)]
+        [ConditionalFact(typeof(RemoteExecutor), nameof(RemoteExecutor.IsSupported))]
+        public static void Options_NullabilityInfoFeatureSwitchDisabled_ReportsPropertiesAsNullable()
+        {
+            var options = new RemoteInvokeOptions()
+            {
+                RuntimeConfigurationOptions =
+                {
+                    ["System.Reflection.NullabilityInfoContext.IsSupported"] = false
+                }
+            };
+
+            RemoteExecutor.Invoke(static () =>
+            {
+                var value = new NullableAnnotationsTests.NotNullablePropertyClass();
+                string expectedJson = """{"Property":null}""";
+
+                Assert.Null(value.Property);
+                string json = JsonSerializer.Serialize(value);
+                Assert.Equal(expectedJson, json);
+                value = JsonSerializer.Deserialize<NullableAnnotationsTests.NotNullablePropertyClass>(json);
+                Assert.Null(value.Property);
+
+            }, options).Dispose();
+        }
+
+        [SkipOnTargetFramework(TargetFrameworkMonikers.NetFramework)]
+        [ConditionalFact(typeof(RemoteExecutor), nameof(RemoteExecutor.IsSupported))]
+        public static void Options_NullabilityInfoFeatureSwitchDisabled_RespectNullabilityAnnotationsEnabled_ThrowsInvalidOperationException()
+        {
+            var options = new RemoteInvokeOptions()
+            {
+                RuntimeConfigurationOptions =
+                {
+                    ["System.Reflection.NullabilityInfoContext.IsSupported"] = false
+                }
+            };
+
+            RemoteExecutor.Invoke(static () =>
+            {
+                var jsonOptions = new JsonSerializerOptions { RespectNullableAnnotations = true };
+                var value = new NullableAnnotationsTests.NotNullablePropertyClass();
+                string expectedJson = """{"Property":null}""";
+                InvalidOperationException ex;
+
+                ex = Assert.Throws<InvalidOperationException>(() => JsonSerializer.Serialize(value, jsonOptions));
+                Assert.Contains("System.Reflection.NullabilityInfoContext.IsSupported", ex.Message);
+
+                ex = Assert.Throws<InvalidOperationException>(() => JsonSerializer.Deserialize<NullableAnnotationsTests.NotNullablePropertyClass>(expectedJson, jsonOptions));
+                Assert.Contains("System.Reflection.NullabilityInfoContext.IsSupported", ex.Message);
+
+            }, options).Dispose();
+        }
+
         private static void GenericObjectOrJsonElementConverterTestHelper<T>(string converterName, object objectValue, string stringValue)
         {
             var options = new JsonSerializerOptions();