diff --git a/dotnet/src/Microsoft.Agents.Orchestration/ConcurrentOrchestration.cs b/dotnet/src/Microsoft.Agents.Orchestration/ConcurrentOrchestration.cs
index 670731efe8..3953b7fd0f 100644
--- a/dotnet/src/Microsoft.Agents.Orchestration/ConcurrentOrchestration.cs
+++ b/dotnet/src/Microsoft.Agents.Orchestration/ConcurrentOrchestration.cs
@@ -61,10 +61,13 @@ public partial class ConcurrentOrchestration : OrchestratingAgent
         this.ResumeAsync(messages, new AgentRunResponse?[this.Agents.Count], context, cancellationToken);
 
     /// <inheritdoc />
-    protected override Task<AgentRunResponse> ResumeCoreAsync(JsonElement checkpointState, OrchestratingAgentContext context, CancellationToken cancellationToken)
+    protected override Task<AgentRunResponse> ResumeCoreAsync(JsonElement checkpointState, IReadOnlyCollection<ChatMessage> newMessages, OrchestratingAgentContext context, CancellationToken cancellationToken)
     {
         var state = checkpointState.Deserialize(OrchestrationJsonContext.Default.ConcurrentState) ?? throw new InvalidOperationException("The checkpoint state is invalid.");
-        return this.ResumeAsync(state.Messages, state.Completed, context, cancellationToken);
+
+        // Append the new messages to the checkpoint state
+        List<ChatMessage> allMessages = [.. state.Messages, .. newMessages];
+        return this.ResumeAsync(allMessages, state.Completed, context, cancellationToken);
     }
 
     /// <inheritdoc />
diff --git a/dotnet/src/Microsoft.Agents.Orchestration/GroupChat/GroupChatOrchestration.cs b/dotnet/src/Microsoft.Agents.Orchestration/GroupChat/GroupChatOrchestration.cs
index 46f258715d..0f0973e768 100644
--- a/dotnet/src/Microsoft.Agents.Orchestration/GroupChat/GroupChatOrchestration.cs
+++ b/dotnet/src/Microsoft.Agents.Orchestration/GroupChat/GroupChatOrchestration.cs
@@ -51,10 +51,14 @@ public sealed partial class GroupChatOrchestration : OrchestratingAgent
     }
 
     /// <inheritdoc />
-    protected override Task<AgentRunResponse> ResumeCoreAsync(JsonElement checkpointState, OrchestratingAgentContext context, CancellationToken cancellationToken)
+    protected override Task<AgentRunResponse> ResumeCoreAsync(JsonElement checkpointState, IReadOnlyCollection<ChatMessage> newMessages, OrchestratingAgentContext context, CancellationToken cancellationToken)
     {
         var state = checkpointState.Deserialize(OrchestrationJsonContext.Default.GroupChatState) ?? throw new InvalidOperationException("The checkpoint state is invalid.");
-        return this.ResumeAsync(state.AllMessages, state.OriginalMessageCount, context, cancellationToken);
+
+        // Append the new messages to the checkpoint state
+        List<ChatMessage> allMessages = [.. state.AllMessages, .. newMessages];
+
+        return this.ResumeAsync(allMessages, allMessages.Count, context, cancellationToken);
     }
 
     private async Task<AgentRunResponse> ResumeAsync(
diff --git a/dotnet/src/Microsoft.Agents.Orchestration/Handoffs/HandoffOrchestration.cs b/dotnet/src/Microsoft.Agents.Orchestration/Handoffs/HandoffOrchestration.cs
index d1c9c5568e..321e71b4a2 100644
--- a/dotnet/src/Microsoft.Agents.Orchestration/Handoffs/HandoffOrchestration.cs
+++ b/dotnet/src/Microsoft.Agents.Orchestration/Handoffs/HandoffOrchestration.cs
@@ -52,26 +52,28 @@ public sealed partial class HandoffOrchestration : OrchestratingAgent
     }
 
     /// <inheritdoc />
-    protected override Task<AgentRunResponse> ResumeCoreAsync(JsonElement checkpointState, OrchestratingAgentContext context, CancellationToken cancellationToken)
+    protected override Task<AgentRunResponse> ResumeCoreAsync(JsonElement checkpointState, IReadOnlyCollection<ChatMessage> newMessages, OrchestratingAgentContext context, CancellationToken cancellationToken)
     {
         var state = checkpointState.Deserialize(OrchestrationJsonContext.Default.HandoffState) ?? throw new InvalidOperationException("The checkpoint state is invalid.");
 
         AIAgent? nextAgent = null;
-        foreach (var agent in this.Agents)
+        if (state.NextAgent is null)
         {
-            if (agent.Id == state.NextAgent)
+            nextAgent = this._handoffs.InitialAgent;
+        }
+        else
+        {
+            nextAgent = this.Agents.FirstOrDefault(a => a.Id == state.NextAgent);
+            if (nextAgent is null)
             {
-                nextAgent = agent;
-                break;
+                Throw.InvalidOperationException($"The next agent '{state.NextAgent}' is not defined in the orchestration.");
             }
         }
 
-        if (nextAgent is null)
-        {
-            Throw.InvalidOperationException($"The next agent '{state.NextAgent}' is not defined in the orchestration.");
-        }
+        // Append the new messages to the checkpoint state
+        List<ChatMessage> allMessages = [.. state.AllMessages, .. newMessages];
 
-        return this.ResumeAsync(nextAgent, state.AllMessages, state.OriginalMessageCount, context, cancellationToken);
+        return this.ResumeAsync(nextAgent, allMessages, allMessages.Count, context, cancellationToken);
     }
 
     /// <inheritdoc />
@@ -144,7 +146,7 @@ public sealed partial class HandoffOrchestration : OrchestratingAgent
     private static void RemoveHandoffFunctionCalls(AgentRunResponse response, List<AITool> handoffTools)
     {
         HashSet<string>? removeToolNames = null;
-        HashSet<string>? callIds = null;
+        HashSet<string>? handoffCallIds = null;
 
         foreach (var message in response.Messages)
         {
@@ -153,23 +155,22 @@ public sealed partial class HandoffOrchestration : OrchestratingAgent
                 if (message.Contents[i] is FunctionCallContent fcc)
                 {
                     removeToolNames ??= [.. handoffTools.Select(t => t.Name)];
-                    (callIds ??= new()).Add(fcc.CallId);
-
                     if (removeToolNames.Contains(fcc.Name))
                     {
+                        (handoffCallIds ??= []).Add(fcc.CallId);
                         message.Contents.RemoveAt(i);
                     }
                 }
             }
         }
 
-        if (callIds is not null)
+        if (handoffCallIds is not null)
         {
             foreach (var message in response.Messages)
             {
                 for (int i = message.Contents.Count - 1; i >= 0; i--)
                 {
-                    if (message.Contents[i] is FunctionResultContent frc && callIds.Contains(frc.CallId))
+                    if (message.Contents[i] is FunctionResultContent frc && handoffCallIds.Contains(frc.CallId))
                     {
                         message.Contents.RemoveAt(i);
                     }
@@ -215,7 +216,7 @@ public sealed partial class HandoffOrchestration : OrchestratingAgent
 
             static void Terminate()
             {
-                if (FunctionInvokingChatClient.CurrentContext is not { } ctx)
+                if (NewFunctionInvokingChatClient.CurrentContext is not { } ctx)
                 {
                     throw new NotSupportedException($"The agent is not configured with a {nameof(FunctionInvokingChatClient)}. Cease execution.");
                 }
diff --git a/dotnet/src/Microsoft.Agents.Orchestration/OrchestratingAgent.cs b/dotnet/src/Microsoft.Agents.Orchestration/OrchestratingAgent.cs
index 733003d8c0..dfbe7bddfe 100644
--- a/dotnet/src/Microsoft.Agents.Orchestration/OrchestratingAgent.cs
+++ b/dotnet/src/Microsoft.Agents.Orchestration/OrchestratingAgent.cs
@@ -135,7 +135,7 @@ public abstract partial class OrchestratingAgent : AIAgent
         JsonElement? checkpoint = await this.ReadCheckpointAsync(context, cancellationToken).ConfigureAwait(false);
         Task<AgentRunResponse> completion = checkpoint is null ?
             this.RunCoreAsync(messages, context, cancellationToken) :
-            this.ResumeCoreAsync(checkpoint.Value, context, cancellationToken);
+            this.ResumeCoreAsync(checkpoint.Value, messages, context, cancellationToken);
 
         if (logger.IsEnabled(LogLevel.Trace))
         {
@@ -157,9 +157,10 @@ public abstract partial class OrchestratingAgent : AIAgent
     /// Resumes processing of the orchestration.
     /// </summary>
     /// <param name="checkpointState">The last checkpoint state available from which to resume the operation.</param>
+    /// <param name="newMessages">The new messages to be processed in addition to the checkpoint state.</param>
     /// <param name="context">The context for this operation.</param>
     /// <param name="cancellationToken">A cancellation token that can be used to cancel the operation.</param>
-    protected abstract Task<AgentRunResponse> ResumeCoreAsync(JsonElement checkpointState, OrchestratingAgentContext context, CancellationToken cancellationToken);
+    protected abstract Task<AgentRunResponse> ResumeCoreAsync(JsonElement checkpointState, IReadOnlyCollection<ChatMessage> newMessages, OrchestratingAgentContext context, CancellationToken cancellationToken);
 
     /// <summary>
     /// Runs the agent with input messages and respond with both streamed and regular messages.
diff --git a/dotnet/src/Microsoft.Agents.Orchestration/OrchestrationJsonContext.cs b/dotnet/src/Microsoft.Agents.Orchestration/OrchestrationJsonContext.cs
index 1ef15b385a..5066f3e6dc 100644
--- a/dotnet/src/Microsoft.Agents.Orchestration/OrchestrationJsonContext.cs
+++ b/dotnet/src/Microsoft.Agents.Orchestration/OrchestrationJsonContext.cs
@@ -1,5 +1,6 @@
 // Copyright (c) Microsoft. All rights reserved.
 
+using System.Text.Json;
 using System.Text.Json.Serialization;
 
 namespace Microsoft.Agents.Orchestration;
@@ -8,4 +9,5 @@ namespace Microsoft.Agents.Orchestration;
 [JsonSerializable(typeof(ConcurrentOrchestration.ConcurrentState))]
 [JsonSerializable(typeof(GroupChatOrchestration.GroupChatState))]
 [JsonSerializable(typeof(HandoffOrchestration.HandoffState))]
+[JsonSerializable(typeof(JsonElement))]
 internal sealed partial class OrchestrationJsonContext : JsonSerializerContext;
diff --git a/dotnet/src/Microsoft.Agents.Orchestration/SequentialOrchestration.cs b/dotnet/src/Microsoft.Agents.Orchestration/SequentialOrchestration.cs
index 6f79bb4129..1c113cfbde 100644
--- a/dotnet/src/Microsoft.Agents.Orchestration/SequentialOrchestration.cs
+++ b/dotnet/src/Microsoft.Agents.Orchestration/SequentialOrchestration.cs
@@ -32,10 +32,13 @@ public sealed partial class SequentialOrchestration : OrchestratingAgent
         this.ResumeAsync(0, messages, context, cancellationToken);
 
     /// <inheritdoc />
-    protected override Task<AgentRunResponse> ResumeCoreAsync(JsonElement checkpointState, OrchestratingAgentContext context, CancellationToken cancellationToken)
+    protected override Task<AgentRunResponse> ResumeCoreAsync(JsonElement checkpointState, IReadOnlyCollection<ChatMessage> newMessages, OrchestratingAgentContext context, CancellationToken cancellationToken)
     {
         var state = checkpointState.Deserialize(OrchestrationJsonContext.Default.SequentialState) ?? throw new InvalidOperationException("The checkpoint state is invalid.");
-        return this.ResumeAsync(state.Index, state.Messages, context, cancellationToken);
+
+        // Append the new messages to the checkpoint state
+        List<ChatMessage> allMessages = [.. state.Messages, .. newMessages];
+        return this.ResumeAsync(state.Index, allMessages, context, cancellationToken);
     }
 
     /// <inheritdoc />
diff --git a/dotnet/tests/Microsoft.Agents.Orchestration.UnitTests/OrchestrationResultTests.cs b/dotnet/tests/Microsoft.Agents.Orchestration.UnitTests/OrchestrationResultTests.cs
index bbc79b661c..9d9f238cca 100644
--- a/dotnet/tests/Microsoft.Agents.Orchestration.UnitTests/OrchestrationResultTests.cs
+++ b/dotnet/tests/Microsoft.Agents.Orchestration.UnitTests/OrchestrationResultTests.cs
@@ -83,7 +83,7 @@ public class OrchestrationResultTests
         protected override Task<AgentRunResponse> RunCoreAsync(IReadOnlyCollection<ChatMessage> messages, OrchestratingAgentContext context, CancellationToken cancellationToken) =>
             throw new NotSupportedException();
 
-        protected override Task<AgentRunResponse> ResumeCoreAsync(JsonElement checkpointState, OrchestratingAgentContext context, CancellationToken cancellationToken) =>
+        protected override Task<AgentRunResponse> ResumeCoreAsync(JsonElement checkpointState, IReadOnlyCollection<ChatMessage> newMessages, OrchestratingAgentContext context, CancellationToken cancellationToken) =>
             throw new NotSupportedException();
     }