diff --git a/src/Aspire.Hosting.RemoteHost/Ats/AtsMarshaller.cs b/src/Aspire.Hosting.RemoteHost/Ats/AtsMarshaller.cs
index 79c9667eb38..7f6a3ee66a9 100644
--- a/src/Aspire.Hosting.RemoteHost/Ats/AtsMarshaller.cs
+++ b/src/Aspire.Hosting.RemoteHost/Ats/AtsMarshaller.cs
@@ -5,6 +5,7 @@
 using System.Reflection;
 using System.Text.Json;
 using System.Text.Json.Nodes;
+using System.Text.Json.Serialization;
 
 namespace Aspire.Hosting.RemoteHost.Ats;
 
@@ -49,7 +50,8 @@ internal sealed class UnmarshalContext
     private static readonly JsonSerializerOptions s_jsonOptions = new()
     {
         PropertyNameCaseInsensitive = true,
-        PropertyNamingPolicy = JsonNamingPolicy.CamelCase
+        PropertyNamingPolicy = JsonNamingPolicy.CamelCase,
+        Converters = { new JsonStringEnumConverter() }
     };
 
     /// <summary>
diff --git a/src/Aspire.Hosting.RemoteHost/Ats/CapabilityDispatcher.cs b/src/Aspire.Hosting.RemoteHost/Ats/CapabilityDispatcher.cs
index 72e29f9d62f..2af40e8523d 100644
--- a/src/Aspire.Hosting.RemoteHost/Ats/CapabilityDispatcher.cs
+++ b/src/Aspire.Hosting.RemoteHost/Ats/CapabilityDispatcher.cs
@@ -533,11 +533,6 @@ private static bool IsTypeMismatchException(ArgumentException ex)
 /// </summary>
 internal static class CapabilityJsonExtensions
 {
-    private static readonly JsonSerializerOptions s_jsonOptions = new()
-    {
-        PropertyNameCaseInsensitive = true,
-        PropertyNamingPolicy = JsonNamingPolicy.CamelCase
-    };
 
     /// <summary>
     /// Gets a required string argument.
@@ -615,7 +610,7 @@ public static T GetRequiredHandle<T>(
     {
         if (args.TryGetPropertyValue(name, out var node) && node is JsonObject obj)
         {
-            return JsonSerializer.Deserialize<T>(obj.ToJsonString(), s_jsonOptions);
+            return JsonSerializer.Deserialize<T>(obj.ToJsonString(), AtsMarshaller.JsonOptions);
         }
         return null;
     }
diff --git a/tests/Aspire.Hosting.RemoteHost.Tests/AtsMarshallerTests.cs b/tests/Aspire.Hosting.RemoteHost.Tests/AtsMarshallerTests.cs
index 77d8793a87e..ff8756b73f8 100644
--- a/tests/Aspire.Hosting.RemoteHost.Tests/AtsMarshallerTests.cs
+++ b/tests/Aspire.Hosting.RemoteHost.Tests/AtsMarshallerTests.cs
@@ -16,7 +16,10 @@ private static AtsContext CreateTestContext()
         {
             Capabilities = [],
             HandleTypes = [],
-            DtoTypes = [new AtsDtoTypeInfo { TypeId = "test/TestDto", Name = "TestDto", ClrType = typeof(TestDto), Properties = [] }],
+            DtoTypes = [
+                new AtsDtoTypeInfo { TypeId = "test/TestDto", Name = "TestDto", ClrType = typeof(TestDto), Properties = [] },
+                new AtsDtoTypeInfo { TypeId = "test/TestDtoWithEnum", Name = "TestDtoWithEnum", ClrType = typeof(TestDtoWithEnum), Properties = [] }
+            ],
             EnumTypes = []
         };
     }
@@ -560,6 +563,56 @@ public void MarshalToJson_MarshalsDto()
         Assert.Equal(10, jsonObj["count"]?.GetValue<int>());
     }
 
+    [Fact]
+    public void JsonOptions_ContainsJsonStringEnumConverter()
+    {
+        var options = AtsMarshaller.JsonOptions;
+
+        Assert.Contains(options.Converters, c => c is System.Text.Json.Serialization.JsonStringEnumConverter);
+    }
+
+    [Fact]
+    public void MarshalToJson_MarshalsDtoWithEnumPropertyAsString()
+    {
+        var marshaller = CreateMarshaller();
+        var dto = new TestDtoWithEnum { Label = "item", Status = TestEnum.ValueB };
+
+        var result = marshaller.MarshalToJson(dto);
+
+        Assert.NotNull(result);
+        Assert.IsType<JsonObject>(result);
+        var jsonObj = (JsonObject)result;
+        Assert.Equal("item", jsonObj["label"]?.GetValue<string>());
+        Assert.Equal("ValueB", jsonObj["status"]?.GetValue<string>());
+    }
+
+    [Fact]
+    public void UnmarshalFromJson_UnmarshalsDtoWithEnumPropertyFromString()
+    {
+        var (marshaller, context) = CreateMarshallerWithContext();
+        var json = new JsonObject { ["label"] = "item", ["status"] = "ValueA" };
+
+        var result = marshaller.UnmarshalFromJson(json, typeof(TestDtoWithEnum), context);
+
+        Assert.NotNull(result);
+        var dto = Assert.IsType<TestDtoWithEnum>(result);
+        Assert.Equal("item", dto.Label);
+        Assert.Equal(TestEnum.ValueA, dto.Status);
+    }
+
+    [Fact]
+    public void UnmarshalFromJson_UnmarshalsDtoWithEnumPropertyCaseInsensitive()
+    {
+        var (marshaller, context) = CreateMarshallerWithContext();
+        var json = new JsonObject { ["label"] = "test", ["status"] = "valueb" };
+
+        var result = marshaller.UnmarshalFromJson(json, typeof(TestDtoWithEnum), context);
+
+        Assert.NotNull(result);
+        var dto = Assert.IsType<TestDtoWithEnum>(result);
+        Assert.Equal(TestEnum.ValueB, dto.Status);
+    }
+
     [Fact]
     public void UnmarshalFromJson_UnmarshalsEnumFromString()
     {
@@ -643,4 +696,11 @@ private sealed class TestDto
         public string? Name { get; set; }
         public int Count { get; set; }
     }
+
+    [AspireDto]
+    private sealed class TestDtoWithEnum
+    {
+        public string? Label { get; set; }
+        public TestEnum Status { get; set; }
+    }
 }
diff --git a/tests/Aspire.Hosting.RemoteHost.Tests/CapabilityDispatcherTests.cs b/tests/Aspire.Hosting.RemoteHost.Tests/CapabilityDispatcherTests.cs
index 6f20ddb2cd6..40becadefb4 100644
--- a/tests/Aspire.Hosting.RemoteHost.Tests/CapabilityDispatcherTests.cs
+++ b/tests/Aspire.Hosting.RemoteHost.Tests/CapabilityDispatcherTests.cs
@@ -1153,6 +1153,53 @@ public void Invoke_AcceptOptionalEnum_WithoutValue()
         Assert.Equal("No value", result.GetValue<string>());
     }
 
+    [Fact]
+    public void GetDto_DeserializesEnumPropertyFromString()
+    {
+        var args = new JsonObject
+        {
+            ["dto"] = new JsonObject
+            {
+                ["label"] = "test-item",
+                ["status"] = "ValueB"
+            }
+        };
+
+        var result = args.GetDto<TestDtoWithEnum>("dto");
+
+        Assert.NotNull(result);
+        Assert.Equal("test-item", result.Label);
+        Assert.Equal(TestDispatchEnum.ValueB, result.Status);
+    }
+
+    [Fact]
+    public void GetDto_DeserializesEnumPropertyFromStringCaseInsensitive()
+    {
+        var args = new JsonObject
+        {
+            ["dto"] = new JsonObject
+            {
+                ["label"] = "item",
+                ["status"] = "valuec"
+            }
+        };
+
+        var result = args.GetDto<TestDtoWithEnum>("dto");
+
+        Assert.NotNull(result);
+        Assert.Equal(TestDispatchEnum.ValueC, result.Status);
+    }
+
+    [Fact]
+    public void GetDto_ReturnsNullWhenPropertyMissing()
+    {
+        var args = new JsonObject();
+
+        var result = args.GetDto<TestDtoWithEnum>("dto");
+
+        Assert.Null(result);
+    }
+
     private static CapabilityDispatcher CreateDispatcher(params System.Reflection.Assembly[] assemblies)
     {
         var handles = new HandleRegistry();
@@ -1431,3 +1478,12 @@ public static string AcceptOptionalEnum(TestDispatchEnum? value = null)
         return value.HasValue ? $"Received: {value.Value}" : "No value";
     }
 }
+
+/// <summary>
+/// Test DTO with an enum property for GetDto deserialization tests.
+/// </summary>
+internal sealed class TestDtoWithEnum
+{
+    public string? Label { get; set; }
+    public TestDispatchEnum Status { get; set; }
+}