diff --git a/src/GrpcHttpApi/src/Microsoft.AspNetCore.Grpc.HttpApi/UnaryServerCallHandler.cs b/src/GrpcHttpApi/src/Microsoft.AspNetCore.Grpc.HttpApi/UnaryServerCallHandler.cs
index 2542fc02f..079fe5606 100644
--- a/src/GrpcHttpApi/src/Microsoft.AspNetCore.Grpc.HttpApi/UnaryServerCallHandler.cs
+++ b/src/GrpcHttpApi/src/Microsoft.AspNetCore.Grpc.HttpApi/UnaryServerCallHandler.cs
@@ -12,7 +12,6 @@
 using System.Threading.Tasks;
 using Google.Protobuf;
 using Google.Protobuf.Reflection;
-using Google.Protobuf.WellKnownTypes;
 using Grpc.Core;
 using Grpc.Gateway.Runtime;
 using Grpc.Shared.HttpApi;
@@ -65,11 +64,17 @@ public UnaryServerCallHandler(
 
         public async Task HandleCallAsync(HttpContext httpContext)
         {
-            var requestMessage = await CreateMessage(httpContext.Request);
+            var selectedEncoding = ResponseEncoding.SelectCharacterEncoding(httpContext.Request);
 
-            var serverCallContext = new HttpApiServerCallContext(httpContext, _unaryMethodInvoker.Method.FullName);
+            var (requestMessage, requestStatusCode, errorMessage) = await CreateMessage(httpContext.Request);
 
-            var selectedEncoding = ResponseEncoding.SelectCharacterEncoding(httpContext.Request);
+            if (requestMessage == null || requestStatusCode != StatusCode.OK)
+            {
+                await SendErrorResponse(httpContext.Response, selectedEncoding, errorMessage ?? string.Empty, requestStatusCode);
+                return;
+            }
+
+            var serverCallContext = new HttpApiServerCallContext(httpContext, _unaryMethodInvoker.Method.FullName);
 
             TResponse responseMessage;
             try
@@ -106,7 +111,7 @@ public async Task HandleCallAsync(HttpContext httpContext)
             await SendResponse(httpContext.Response, selectedEncoding, responseMessage);
         }
 
-        private async Task<IMessage> CreateMessage(HttpRequest request)
+        private async Task<(IMessage? requestMessage, StatusCode statusCode, string? errorMessage)> CreateMessage(HttpRequest request)
         {
             IMessage? requestMessage;
 
@@ -115,7 +120,7 @@ private async Task<IMessage> CreateMessage(HttpRequest request)
                 if (request.ContentType == null ||
                     !request.ContentType.StartsWith("application/json", StringComparison.OrdinalIgnoreCase))
                 {
-                    throw new InvalidOperationException("Request content-type of application/json is required.");
+                    return (null, StatusCode.InvalidArgument, "Request content-type of application/json is required.");
                 }
 
                 if (!request.Body.CanSeek)
@@ -150,7 +155,20 @@ private async Task<IMessage> CreateMessage(HttpRequest request)
                     }
                     else
                     {
-                        var bodyContent = JsonParser.Default.Parse(requestReader, _bodyDescriptor);
+                        IMessage bodyContent;
+
+                        try
+                        {
+                            bodyContent = JsonParser.Default.Parse(requestReader, _bodyDescriptor);
+                        }
+                        catch (InvalidJsonException)
+                        {
+                            return (null, StatusCode.InvalidArgument, "Request JSON payload is not correctly formatted.");
+                        }
+                        catch (InvalidProtocolBufferException exception)
+                        {
+                            return (null, StatusCode.InvalidArgument, exception.Message);
+                        }
 
                         if (_bodyFieldDescriptors != null)
                         {
@@ -192,7 +210,7 @@ private async Task<IMessage> CreateMessage(HttpRequest request)
                 }
             }
 
-            return requestMessage;
+            return (requestMessage, StatusCode.OK, null);
         }
 
         private List<FieldDescriptor>? GetPathDescriptors(IMessage requestMessage, string path)
diff --git a/src/GrpcHttpApi/test/Microsoft.AspNetCore.Grpc.HttpApi.Tests/UnaryServerCallHandlerTests.cs b/src/GrpcHttpApi/test/Microsoft.AspNetCore.Grpc.HttpApi.Tests/UnaryServerCallHandlerTests.cs
index 5204b18fc..c99abc4f0 100644
--- a/src/GrpcHttpApi/test/Microsoft.AspNetCore.Grpc.HttpApi.Tests/UnaryServerCallHandlerTests.cs
+++ b/src/GrpcHttpApi/test/Microsoft.AspNetCore.Grpc.HttpApi.Tests/UnaryServerCallHandlerTests.cs
@@ -336,6 +336,68 @@ public async Task HandleCallAsync_MatchingQueryStringValues_SetOnRequestMessage(
             Assert.Equal("TestSubfield!", request!.Sub.Subfield);
         }
 
+        [Theory]
+        [InlineData("{malformed_json}", "Request JSON payload is not correctly formatted.")]
+        [InlineData("{\"name\": 1234}", "Unsupported conversion from JSON number for field type String")]
+        [InlineData("{\"abcd\": 1234}", "Unknown field: abcd")]
+        public async Task HandleCallAsync_MalformedRequestBody_BadRequestReturned(string json, string expectedError)
+        {
+            // Arrange
+            UnaryServerMethod<HttpApiGreeterService, HelloRequest, HelloReply> invoker = (s, r, c) =>
+            {
+                return Task.FromResult(new HelloReply());
+            };
+
+            var unaryServerCallHandler = CreateCallHandler(
+                invoker,
+                bodyDescriptor: HelloRequest.Descriptor);
+            var httpContext = CreateHttpContext();
+            httpContext.Request.Body = new MemoryStream(Encoding.UTF8.GetBytes(json));
+            httpContext.Request.ContentType = "application/json";
+            // Act
+            await unaryServerCallHandler.HandleCallAsync(httpContext);
+
+            // Assert
+            Assert.Equal(400, httpContext.Response.StatusCode);
+
+            httpContext.Response.Body.Seek(0, SeekOrigin.Begin);
+            using var responseJson = JsonDocument.Parse(httpContext.Response.Body);
+            Assert.Equal(expectedError, responseJson.RootElement.GetProperty("message").GetString());
+            Assert.Equal(expectedError, responseJson.RootElement.GetProperty("error").GetString());
+            Assert.Equal((int)StatusCode.InvalidArgument, responseJson.RootElement.GetProperty("code").GetInt32());
+        }
+
+        [Theory]
+        [InlineData(null)]
+        [InlineData("text/html")]
+        public async Task HandleCallAsync_BadContentType_BadRequestReturned(string contentType)
+        {
+            // Arrange
+            UnaryServerMethod<HttpApiGreeterService, HelloRequest, HelloReply> invoker = (s, r, c) =>
+            {
+                return Task.FromResult(new HelloReply());
+            };
+
+            var unaryServerCallHandler = CreateCallHandler(
+                invoker,
+                bodyDescriptor: HelloRequest.Descriptor);
+            var httpContext = CreateHttpContext();
+            httpContext.Request.Body = new MemoryStream(Encoding.UTF8.GetBytes("{}"));
+            httpContext.Request.ContentType = contentType;
+            // Act
+            await unaryServerCallHandler.HandleCallAsync(httpContext);
+
+            // Assert
+            Assert.Equal(400, httpContext.Response.StatusCode);
+
+            var expectedError = "Request content-type of application/json is required.";
+            httpContext.Response.Body.Seek(0, SeekOrigin.Begin);
+            using var responseJson = JsonDocument.Parse(httpContext.Response.Body);
+            Assert.Equal(expectedError, responseJson.RootElement.GetProperty("message").GetString());
+            Assert.Equal(expectedError, responseJson.RootElement.GetProperty("error").GetString());
+            Assert.Equal((int)StatusCode.InvalidArgument, responseJson.RootElement.GetProperty("code").GetInt32());
+        }
+
         [Fact]
         public async Task HandleCallAsync_RpcExceptionReturned_StatusReturned()
         {