diff --git a/src/libraries/System.Text.Json/gen/Helpers/RoslynExtensions.cs b/src/libraries/System.Text.Json/gen/Helpers/RoslynExtensions.cs
index 5512321b0e2f04..3701b263a315bc 100644
--- a/src/libraries/System.Text.Json/gen/Helpers/RoslynExtensions.cs
+++ b/src/libraries/System.Text.Json/gen/Helpers/RoslynExtensions.cs
@@ -323,7 +323,7 @@ public static bool IsNullable(this IParameterSymbol parameter)
             {
                 // Because System.Text.Json cannot distinguish between nullable and non-nullable type parameters,
                 // (e.g. the same metadata is being used for both KeyValuePair<string, string?> and KeyValuePair<string, string>),
-                // we derive nullability annotations from the original definition of the field and not instation.
+                // we derive nullability annotations from the original definition of the field and not its instantiation.
                 // This preserves compatibility with the capabilities of the reflection-based NullabilityInfo reader.
                 parameter = parameter.OriginalDefinition;
                 return !IsInputTypeNonNullable(parameter, parameter.Type);
diff --git a/src/libraries/System.Text.Json/gen/JsonSourceGenerator.Emitter.cs b/src/libraries/System.Text.Json/gen/JsonSourceGenerator.Emitter.cs
index 11bf6ae9f3cf6a..f2de4d1b063083 100644
--- a/src/libraries/System.Text.Json/gen/JsonSourceGenerator.Emitter.cs
+++ b/src/libraries/System.Text.Json/gen/JsonSourceGenerator.Emitter.cs
@@ -754,6 +754,7 @@ private static void GenerateCtorParamMetadataInitFunc(SourceWriter writer, strin
                             Name = {{FormatStringLiteral(spec.Name)}},
                             ParameterType = typeof({{spec.ParameterType.FullyQualifiedName}}),
                             Position = {{spec.ParameterIndex}},
+                            IsNullable = {{FormatBoolLiteral(spec.IsNullable)}},
                             IsMemberInitializer = true,
                         },
                         """);
diff --git a/src/libraries/System.Text.Json/gen/JsonSourceGenerator.Parser.cs b/src/libraries/System.Text.Json/gen/JsonSourceGenerator.Parser.cs
index d7c9bc72041b29..d63669f2eacf52 100644
--- a/src/libraries/System.Text.Json/gen/JsonSourceGenerator.Parser.cs
+++ b/src/libraries/System.Text.Json/gen/JsonSourceGenerator.Parser.cs
@@ -1534,6 +1534,7 @@ private void ProcessMember(
                                 ParameterType = property.PropertyType,
                                 MatchesConstructorParameter = matchingConstructorParameter is not null,
                                 ParameterIndex = matchingConstructorParameter?.ParameterIndex ?? paramCount++,
+                                IsNullable = property.PropertyType.CanBeNull && !property.IsSetterNonNullableAnnotation,
                             };
 
                             (propertyInitializers ??= new()).Add(propertyInitializer);
diff --git a/src/libraries/System.Text.Json/gen/Model/PropertyInitializerGenerationSpec.cs b/src/libraries/System.Text.Json/gen/Model/PropertyInitializerGenerationSpec.cs
index 608ce8e887d725..189dac1784e4f1 100644
--- a/src/libraries/System.Text.Json/gen/Model/PropertyInitializerGenerationSpec.cs
+++ b/src/libraries/System.Text.Json/gen/Model/PropertyInitializerGenerationSpec.cs
@@ -31,5 +31,7 @@ public sealed record PropertyInitializerGenerationSpec
         public required int ParameterIndex { get; init; }
 
         public required bool MatchesConstructorParameter { get; init; }
+
+        public required bool IsNullable { get; init; }
     }
 }
diff --git a/src/libraries/System.Text.Json/tests/Common/NullableAnnotationsTests.cs b/src/libraries/System.Text.Json/tests/Common/NullableAnnotationsTests.cs
index 6ad6cad83c6258..5ce2030301c0f9 100644
--- a/src/libraries/System.Text.Json/tests/Common/NullableAnnotationsTests.cs
+++ b/src/libraries/System.Text.Json/tests/Common/NullableAnnotationsTests.cs
@@ -72,6 +72,8 @@ public static IEnumerable<object[]> GetTypesWithNonNullablePropertyGetter()
             yield return Wrap(typeof(NotNullableSpecialTypePropertiesClass), nameof(NotNullableSpecialTypePropertiesClass.JsonDocument));
             yield return Wrap(typeof(NullableObliviousConstructorParameter), nameof(NullableObliviousConstructorParameter.Property));
             yield return Wrap(typeof(NotNullGenericPropertyClass<string>), nameof(NotNullGenericPropertyClass<string>.Property));
+            yield return Wrap(typeof(ClassWithNonNullableInitProperty), nameof(ClassWithNonNullableInitProperty.Property));
+            yield return Wrap(typeof(ClassWithNonNullableInitProperty), nameof(ClassWithNonNullableRequiredProperty.Property));
 
             static object[] Wrap(Type type, string propertyName) => [type, propertyName];
         }
@@ -125,6 +127,8 @@ public static IEnumerable<object[]> GetTypesWithNullablePropertyGetter()
             yield return Wrap(typeof(NullableObliviousPropertyClass), nameof(NullableObliviousPropertyClass.Property));
             yield return Wrap(typeof(GenericPropertyClass<string>), nameof(GenericPropertyClass<string>.Property));
             yield return Wrap(typeof(NullableGenericPropertyClass<string>), nameof(NullableGenericPropertyClass<string>.Property));
+            yield return Wrap(typeof(ClassWithNullableInitProperty), nameof(ClassWithNullableInitProperty.Property));
+            yield return Wrap(typeof(ClassWithNullableInitProperty), nameof(ClassWithNullableRequiredProperty.Property));
 
             static object[] Wrap(Type type, string propertyName) => [type, propertyName];
         }
@@ -191,6 +195,8 @@ public static IEnumerable<object[]> GetTypesWithNonNullablePropertySetter()
             yield return Wrap(typeof(DisallowNullConstructorParameter), nameof(DisallowNullConstructorParameter.Property));
             yield return Wrap(typeof(DisallowNullConstructorParameter<string>), nameof(DisallowNullConstructorParameter<string>.Property));
             yield return Wrap(typeof(NotNullGenericConstructorParameter<string>), nameof(NotNullGenericConstructorParameter<string>.Property));
+            yield return Wrap(typeof(ClassWithNonNullableInitProperty), nameof(ClassWithNonNullableInitProperty.Property));
+            yield return Wrap(typeof(ClassWithNonNullableInitProperty), nameof(ClassWithNonNullableRequiredProperty.Property));
 
             static object[] Wrap(Type type, string propertyName) => [type, propertyName];
         }
@@ -249,6 +255,8 @@ public static IEnumerable<object[]> GetTypesWithNullablePropertySetter()
             yield return Wrap(typeof(AllowNullConstructorParameter<string>), nameof(AllowNullConstructorParameter<string>.Property));
             yield return Wrap(typeof(GenericConstructorParameter<string>), nameof(GenericConstructorParameter<string>.Property));
             yield return Wrap(typeof(NullableGenericConstructorParameter<string>), nameof(NullableGenericConstructorParameter<string>.Property));
+            yield return Wrap(typeof(ClassWithNullableInitProperty), nameof(ClassWithNullableInitProperty.Property));
+            yield return Wrap(typeof(ClassWithNullableInitProperty), nameof(ClassWithNullableRequiredProperty.Property));
 
             static object[] Wrap(Type type, string propertyName) => [type, propertyName];
         }
@@ -765,5 +773,25 @@ public class NullableFieldClass
             [JsonInclude]
             public string? Field;
         }
+
+        public class ClassWithNullableInitProperty
+        {
+            public string? Property { get; init; }
+        }
+
+        public class ClassWithNonNullableInitProperty
+        {
+            public string Property { get; init; }
+        }
+
+        public class ClassWithNullableRequiredProperty
+        {
+            public required string? Property { get; set; }
+        }
+
+        public class ClassWithNonNullableRequiredProperty
+        {
+            public required string Property { get; set; }
+        }
     }
 }
diff --git a/src/libraries/System.Text.Json/tests/System.Text.Json.SourceGeneration.Tests/Serialization/NullableAnnotationsTests.cs b/src/libraries/System.Text.Json/tests/System.Text.Json.SourceGeneration.Tests/Serialization/NullableAnnotationsTests.cs
index 33fdc55b8a1d37..663229c132e6ef 100644
--- a/src/libraries/System.Text.Json/tests/System.Text.Json.SourceGeneration.Tests/Serialization/NullableAnnotationsTests.cs
+++ b/src/libraries/System.Text.Json/tests/System.Text.Json.SourceGeneration.Tests/Serialization/NullableAnnotationsTests.cs
@@ -65,6 +65,10 @@ protected NullableAnnotationsTests_Metadata(JsonSerializerWrapper serializer)
         [JsonSerializable(typeof(NullableGenericConstructorParameter<string>))]
         [JsonSerializable(typeof(NotNullGenericConstructorParameter<string>))]
         [JsonSerializable(typeof(NotNullablePropertyWithIgnoreConditions))]
+        [JsonSerializable(typeof(ClassWithNullableInitProperty))]
+        [JsonSerializable(typeof(ClassWithNonNullableInitProperty))]
+        [JsonSerializable(typeof(ClassWithNullableRequiredProperty))]
+        [JsonSerializable(typeof(ClassWithNonNullableRequiredProperty))]
         internal sealed partial class NullableAnnotationsTestsContext_Metadata
             : JsonSerializerContext { }
     }
@@ -128,6 +132,10 @@ protected NullableAnnotationsTests_Default(JsonSerializerWrapper serializer)
         [JsonSerializable(typeof(NullableGenericConstructorParameter<string>))]
         [JsonSerializable(typeof(NotNullGenericConstructorParameter<string>))]
         [JsonSerializable(typeof(NotNullablePropertyWithIgnoreConditions))]
+        [JsonSerializable(typeof(ClassWithNullableInitProperty))]
+        [JsonSerializable(typeof(ClassWithNonNullableInitProperty))]
+        [JsonSerializable(typeof(ClassWithNullableRequiredProperty))]
+        [JsonSerializable(typeof(ClassWithNonNullableRequiredProperty))]
         internal sealed partial class NullableAnnotationsTestsContext_Default
             : JsonSerializerContext
         { }