diff --git a/dotnet/src/Microsoft.AutoGen/RuntimeGateway.Grpc/Services/Orleans/MessageRegistryGrain.cs b/dotnet/src/Microsoft.AutoGen/RuntimeGateway.Grpc/Services/Orleans/MessageRegistryGrain.cs
index 59dec750d..534114920 100644
--- a/dotnet/src/Microsoft.AutoGen/RuntimeGateway.Grpc/Services/Orleans/MessageRegistryGrain.cs
+++ b/dotnet/src/Microsoft.AutoGen/RuntimeGateway.Grpc/Services/Orleans/MessageRegistryGrain.cs
@@ -12,10 +12,14 @@ internal sealed class MessageRegistryGrain(
     ILogger<MessageRegistryGrain> logger
 ) : Grain, IMessageRegistryGrain
 {
+    // <summary>
+    // Helper class for managing state writes.
+    // </summary>
+    private readonly StateManager _stateManager = new(state);
+
     // <summary>
     // The number of times to retry writing the state before giving up.
     // </summary>
-
     private const int _retries = 5;
     /// <summary>
     /// The time to wait before removing a message from the event buffer.
@@ -35,12 +39,9 @@ internal sealed class MessageRegistryGrain(
     {
         await TryWriteMessageAsync("eb", topic, message).ConfigureAwait(true);
         // Schedule the removal task to run in the background after bufferTime
-        _ = Task.Delay(_bufferTime)
-            .ContinueWith(
-                async _ => await RemoveMessage(topic, message),
-                TaskScheduler.Default
-            );
+        RemoveMessageAfterDelay(topic, message).Ignore();
     }
+
     /// <summary>
     /// remove a specific message from the buffer for a given topic
     /// </summary>
@@ -54,13 +55,24 @@ internal sealed class MessageRegistryGrain(
             if (events != null && events.Remove(message))
             {
                 state.State.EventBuffer.AddOrUpdate(topic, events, (_, _) => events);
-                await state.WriteStateAsync().ConfigureAwait(true);
+                await _stateManager.WriteStateAsync().ConfigureAwait(true);
                 return true;
             }
         }
         return false;
     }
 
+    /// <summary>
+    /// remove a specific message from the buffer for a given topic after a delay
+    /// </summary>
+    /// <param name="topic"></param>
+    /// <param name="message"></param>
+    private async Task RemoveMessageAfterDelay(string topic, CloudEvent message)
+    {
+        await Task.Delay(_bufferTime);
+        await RemoveMessage(topic, message);
+    }
+
     /// <summary>
     /// Tries to write a message to the given queue in Orleans state.
     /// Allows for retries using etag for optimistic concurrency.
@@ -114,7 +126,7 @@ internal sealed class MessageRegistryGrain(
             default:
                 throw new ArgumentException($"Invalid queue name: {whichQueue}");
         }
-        await state.WriteStateAsync().ConfigureAwait(true);
+        await _stateManager.WriteStateAsync().ConfigureAwait(true);
         return true;
     }
 
@@ -124,7 +136,7 @@ internal sealed class MessageRegistryGrain(
         var messages = new List<CloudEvent>();
         if (state.State.DeadLetterQueue != null && state.State.DeadLetterQueue.Remove(topic, out List<CloudEvent>? letters))
         {
-            await state.WriteStateAsync().ConfigureAwait(true);
+            await _stateManager.WriteStateAsync().ConfigureAwait(true);
             if (letters != null)
             {
                 messages.AddRange(letters);
@@ -132,7 +144,7 @@ internal sealed class MessageRegistryGrain(
         }
         if (state.State.EventBuffer != null && state.State.EventBuffer.Remove(topic, out List<CloudEvent>? events))
         {
-            await state.WriteStateAsync().ConfigureAwait(true);
+            await _stateManager.WriteStateAsync().ConfigureAwait(true);
             if (events != null)
             {
                 messages.AddRange(events);
diff --git a/dotnet/src/Microsoft.AutoGen/RuntimeGateway.Grpc/Services/Orleans/StateManager.cs b/dotnet/src/Microsoft.AutoGen/RuntimeGateway.Grpc/Services/Orleans/StateManager.cs
new file mode 100644
index 000000000..6c022d1c0
--- /dev/null
+++ b/dotnet/src/Microsoft.AutoGen/RuntimeGateway.Grpc/Services/Orleans/StateManager.cs
@@ -0,0 +1,74 @@
+// Copyright (c) Microsoft Corporation. All rights reserved.
+// StateManager.cs
+
+using Orleans.Core;
+
+namespace Microsoft.AutoGen.RuntimeGateway.Grpc;
+
+/// <summary>
+/// A helper class which wraps a grain state instance and ensures that only a single write operation is outstanding at any moment in time.
+/// </summary>
+/// <param name="state">The grain state.</param>
+internal sealed class StateManager(IStorage state)
+{
+    /// <summary>
+    /// Allows state writing to happen in the background.
+    /// </summary>
+    private Task? _pendingOperation;
+
+    // When reentrant grain is doing WriteStateAsync, etag violations are possible due to concurrent writes.
+    // The solution is to serialize and batch writes, and make sure only a single write is outstanding at any moment in time.
+    public async ValueTask WriteStateAsync()
+    {
+        await PerformOperationAsync(static state => state.WriteStateAsync());
+    }
+
+    public async ValueTask ClearStateAsync()
+    {
+        await PerformOperationAsync(static state => state.ClearStateAsync());
+    }
+
+    public async ValueTask PerformOperationAsync(Func<IStorage, Task> performOperation)
+    {
+        if (_pendingOperation is Task currentWriteStateOperation)
+        {
+            // await the outstanding write, but ignore it since it doesn't include our changes
+            await currentWriteStateOperation.ConfigureAwait(ConfigureAwaitOptions.SuppressThrowing | ConfigureAwaitOptions.ContinueOnCapturedContext);
+            if (_pendingOperation == currentWriteStateOperation)
+            {
+                // only null out the outstanding operation if it's the same one as the one we awaited, otherwise
+                // another request might have already done so.
+                _pendingOperation = null;
+            }
+        }
+
+        Task operation;
+        if (_pendingOperation is null)
+        {
+            // If after the initial write is completed, no other request initiated a new write operation, do it now.
+            operation = performOperation(state);
+            _pendingOperation = operation;
+        }
+        else
+        {
+            // If there were many requests enqueued to persist state, there is no reason to enqueue a new write 
+            // operation for each, since any write (after the initial one that we already awaited) will have cumulative
+            // changes including the one requested by our caller. Just await the new outstanding write.
+            operation = _pendingOperation;
+        }
+
+        try
+        {
+            await operation;
+        }
+        finally
+        {
+            if (_pendingOperation == operation)
+            {
+                // only null out the outstanding operation if it's the same one as the one we awaited, otherwise
+                // another request might have already done so.
+                _pendingOperation = null;
+            }
+        }
+    }
+}