diff --git a/src/StreamJsonRpc/Reflection/MessageFormatterEnumerableTracker.cs b/src/StreamJsonRpc/Reflection/MessageFormatterEnumerableTracker.cs
index defcf4164..bb38835d9 100644
--- a/src/StreamJsonRpc/Reflection/MessageFormatterEnumerableTracker.cs
+++ b/src/StreamJsonRpc/Reflection/MessageFormatterEnumerableTracker.cs
@@ -39,8 +39,15 @@ public class MessageFormatterEnumerableTracker
     private static readonly MethodInfo OnDisposeAsyncMethodInfo = typeof(MessageFormatterEnumerableTracker).GetMethod(nameof(OnDisposeAsync), BindingFlags.NonPublic | BindingFlags.Instance)!;
 
     /// <summary>
-    /// Dictionary used to map the outbound request id to their progress info so that the progress objects are cleaned after getting the final response.
+    /// Dictionary used to map the outbound request id to the list of tokens that track <see cref="IAsyncEnumerable{T}"/> state machines it owns
+    /// so that the state machines are cleaned after getting the final response.
     /// </summary>
+    /// <remarks>
+    /// Note that we only track OUTBOUND REQUESTS that carry enumerables here.
+    /// OUTBOUND RESPONSES that carry enumerables are not tracked except in <see cref="generatorsByToken"/>.
+    /// This means that responses that carry enumerables will not be cleaned up if the response is never processed by the client
+    /// until the connection dies.
+    /// </remarks>
     private readonly Dictionary<RequestId, ImmutableList<long>> generatorTokensByRequestId = new Dictionary<RequestId, ImmutableList<long>>();
 
     private readonly Dictionary<long, IGeneratingEnumeratorTracker> generatorsByToken = new Dictionary<long, IGeneratingEnumeratorTracker>();
@@ -116,12 +123,20 @@ public long GetToken<T>(IAsyncEnumerable<T> enumerable)
         long handle = Interlocked.Increment(ref this.nextToken);
         lock (this.syncObject)
         {
-            if (!this.generatorTokensByRequestId.TryGetValue(this.formatterState.SerializingMessageWithId, out ImmutableList<long>? tokens))
+            // We only track the token if we are serializing a request, since per our documentation,
+            // we forcibly terminate the enumerable at the client side when the request has been responded to.
+            // Storing request IDs for outbound *responses* that carry enumerables would lead to them being disposed of
+            // when an INBOUND response with the same ID is received.
+            if (this.formatterState.SerializingRequest)
             {
-                tokens = ImmutableList<long>.Empty;
+                if (!this.generatorTokensByRequestId.TryGetValue(this.formatterState.SerializingMessageWithId, out ImmutableList<long>? tokens))
+                {
+                    tokens = ImmutableList<long>.Empty;
+                }
+
+                this.generatorTokensByRequestId[this.formatterState.SerializingMessageWithId] = tokens.Add(handle);
             }
 
-            this.generatorTokensByRequestId[this.formatterState.SerializingMessageWithId] = tokens.Add(handle);
             this.generatorsByToken.Add(handle, new GeneratingEnumeratorTracker<T>(this, handle, enumerable, settings: enumerable.GetJsonRpcSettings()));
         }
 
@@ -173,18 +188,18 @@ private ValueTask OnDisposeAsync(long token)
         return generator.DisposeAsync();
     }
 
-    private void CleanUpResources(RequestId requestId)
+    private void CleanUpResources(RequestId outboundRequestId)
     {
         lock (this.syncObject)
         {
-            if (this.generatorTokensByRequestId.TryGetValue(requestId, out ImmutableList<long>? tokens))
+            if (this.generatorTokensByRequestId.TryGetValue(outboundRequestId, out ImmutableList<long>? tokens))
             {
                 foreach (var token in tokens)
                 {
                     this.generatorsByToken.Remove(token);
                 }
 
-                this.generatorTokensByRequestId.Remove(requestId);
+                this.generatorTokensByRequestId.Remove(outboundRequestId);
             }
         }
     }
diff --git a/test/StreamJsonRpc.Tests/AsyncEnumerableTests.cs b/test/StreamJsonRpc.Tests/AsyncEnumerableTests.cs
index 6cbe8a40c..7d884573e 100644
--- a/test/StreamJsonRpc.Tests/AsyncEnumerableTests.cs
+++ b/test/StreamJsonRpc.Tests/AsyncEnumerableTests.cs
@@ -11,17 +11,17 @@
 using Microsoft.VisualStudio.Threading;
 using Nerdbank.Streams;
 using Newtonsoft.Json;
-using StreamJsonRpc;
-using Xunit;
-using Xunit.Abstractions;
 
 public abstract class AsyncEnumerableTests : TestBase, IAsyncLifetime
 {
-    protected readonly Server server = new Server();
+    protected readonly Server server = new();
+    protected readonly Client client = new();
+
     protected JsonRpc serverRpc;
     protected IJsonRpcMessageFormatter serverMessageFormatter;
 
     protected Lazy<IServer> clientProxy;
+    protected Lazy<IClient> serverProxy;
     protected JsonRpc clientRpc;
     protected IJsonRpcMessageFormatter clientMessageFormatter;
 
@@ -73,6 +73,13 @@ protected interface IServer
         Task PassInNumbersAndIgnoreAsync(IAsyncEnumerable<int> numbers, CancellationToken cancellationToken);
 
         Task PassInNumbersOnlyStartEnumerationAsync(IAsyncEnumerable<int> numbers, CancellationToken cancellationToken);
+
+        IAsyncEnumerable<string> CallbackClientAndYieldOneValueAsync(CancellationToken cancellationToken);
+    }
+
+    protected interface IClient
+    {
+        Task DoSomethingAsync(CancellationToken cancellationToken);
     }
 
     public Task InitializeAsync()
@@ -85,7 +92,7 @@ public Task InitializeAsync()
         var clientHandler = new LengthHeaderMessageHandler(streams.Item2.UsePipe(), this.clientMessageFormatter);
 
         this.serverRpc = new JsonRpc(serverHandler, this.server);
-        this.clientRpc = new JsonRpc(clientHandler);
+        this.clientRpc = new JsonRpc(clientHandler, this.client);
 
         this.serverRpc.TraceSource = new TraceSource("Server", SourceLevels.Verbose);
         this.clientRpc.TraceSource = new TraceSource("Client", SourceLevels.Verbose);
@@ -97,6 +104,7 @@ public Task InitializeAsync()
         this.clientRpc.StartListening();
 
         this.clientProxy = new Lazy<IServer>(() => this.clientRpc.Attach<IServer>());
+        this.serverProxy = new Lazy<IClient>(() => this.serverRpc.Attach<IClient>());
 
         return Task.CompletedTask;
     }
@@ -530,6 +538,17 @@ public async Task AsyncIteratorThrows(int minBatchSize, int maxReadAhead, int pr
         Assert.Equal(Server.FailByDesignExceptionMessage, ex.Message);
     }
 
+    [Fact]
+    public async Task EnumerableIdDisposal()
+    {
+        // This test is specially arranged to create two RPC calls going opposite directions, with the same request ID.
+        // By doing so, we can verify that the server doesn't dispose the enumerable until the full sequence is sent to the client.
+        this.server.Client = this.serverProxy.Value;
+        await foreach (string s in this.clientProxy.Value.CallbackClientAndYieldOneValueAsync(this.TimeoutToken))
+        {
+        }
+    }
+
     protected abstract void InitializeFormattersAndHandlers();
 
     private static void AssertCollectedObject(WeakReference weakReference)
@@ -621,6 +640,8 @@ protected class Server : IServer
 
         internal const string FailByDesignExceptionMessage = "Fail by design";
 
+        public IClient? Client { get; set; }
+
         public AsyncManualResetEvent MethodEntered { get; } = new AsyncManualResetEvent();
 
         public AsyncManualResetEvent MethodExited { get; } = new AsyncManualResetEvent();
@@ -745,6 +766,18 @@ public Task<CompoundEnumerableResult> GetNumbersAndMetadataAsync(CancellationTok
             });
         }
 
+        public async IAsyncEnumerable<string> CallbackClientAndYieldOneValueAsync([EnumeratorCancellation] CancellationToken cancellationToken)
+        {
+            if (this.Client is null)
+            {
+                throw new InvalidOperationException("Client must be set before calling this method.");
+            }
+
+            // We deliberately make a callback right away such that the request ID for it collides with the request ID that served THIS request.
+            await this.Client.DoSomethingAsync(cancellationToken);
+            yield return "Hello";
+        }
+
         private async IAsyncEnumerable<int> GetNumbersAsync(int totalCount, bool endWithException, [EnumeratorCancellation] CancellationToken cancellationToken)
         {
             for (int i = 1; i <= totalCount; i++)
@@ -763,6 +796,11 @@ private async IAsyncEnumerable<int> GetNumbersAsync(int totalCount, bool endWith
         }
     }
 
+    protected class Client : IClient
+    {
+        public Task DoSomethingAsync(CancellationToken cancellationToken) => Task.CompletedTask;
+    }
+
     [DataContract]
     protected class CompoundEnumerableResult
     {