diff --git a/src/ZendeskApi.Client/Exceptions/ErrorWithMessageResponse.cs b/src/ZendeskApi.Client/Exceptions/ErrorWithMessageResponse.cs
new file mode 100644
index 00000000..5f460e9b
--- /dev/null
+++ b/src/ZendeskApi.Client/Exceptions/ErrorWithMessageResponse.cs
@@ -0,0 +1,38 @@
+using Newtonsoft.Json;
+using Newtonsoft.Json.Linq;
+
+namespace ZendeskApi.Client.Exceptions
+{
+    /// <summary />
+    public class ErrorWithMessageResponse
+    {
+        /// <summary />
+        public ErrorWithMessageResponse()
+        {
+        }
+
+        /// <summary />
+        [JsonProperty("error")]
+        public ErrorWithMessage Error { get; internal set; }
+
+        /// <summary />
+        public ErrorResponse ToErrorResponse(JObject details = null) => new ErrorResponse()
+        {
+            Error       = Error?.Title,
+            Description = Error?.Message,
+            Details     = details
+        };
+
+        /// <summary />
+        public class ErrorWithMessage()
+        {
+            /// <summary />
+            [JsonProperty("message")]
+            public string Message { get; internal set; }
+
+            /// <summary />
+            [JsonProperty("title")]
+            public string Title { get; internal set; }
+        }
+    }
+}
diff --git a/src/ZendeskApi.Client/Exceptions/ZendeskRequestExceptionBuilder.cs b/src/ZendeskApi.Client/Exceptions/ZendeskRequestExceptionBuilder.cs
index afdfd862..9993c0fe 100644
--- a/src/ZendeskApi.Client/Exceptions/ZendeskRequestExceptionBuilder.cs
+++ b/src/ZendeskApi.Client/Exceptions/ZendeskRequestExceptionBuilder.cs
@@ -59,12 +59,39 @@ public async Task<ZendeskRequestException> Build()
                 (int)_response.StatusCode <= 499 && 
                 !_doNotBuildErrorModelResponseCodes.Contains((int)_response.StatusCode))
             {
-                error = await _response.Content.ReadAsAsync<ErrorResponse>();
+                var content = await _response.Content.ReadAsStringAsync();
 
+                try
+                {
+                    error = JsonConvert.DeserializeObject<ErrorResponse>(content);
+                }
+                catch (JsonReaderException)
+                {
+                    try
+                    {
+                        error = JsonConvert.DeserializeObject<ErrorWithMessageResponse>(content)?.ToErrorResponse();
+                    }
+                    catch
+                    { 
+                        // Swallow a deserialization failure here.
+                    }
+
+                    // Throw the original exception if an error could not be deserialized.
+                    if ( error == null )
+                        throw;
+                }
+               
                 if (error?.Error != null && error.Description != null)
                 {
-                    var detail = Environment.NewLine + JsonConvert.SerializeObject(error.Details, Formatting.Indented);
-                    message.AppendLine($"{error.Error}: {error.Description}. {detail}");
+                    if (error.Details == null)
+                    {
+                        message.AppendLine($"{error.Error}: {error.Description.TrimEnd('.')}.");
+                    }
+                    else
+                    {
+                        var detail = Environment.NewLine + JsonConvert.SerializeObject(error.Details, Formatting.Indented);
+                        message.AppendLine($"{error.Error}: {error.Description}. {detail}");
+                    }
                 }
             }