diff --git a/src/ProjectTemplates/Microsoft.Extensions.AI.Templates/src/ChatWithCustomData/ChatWithCustomData-CSharp.Web/Components/Pages/Chat/Chat.razor b/src/ProjectTemplates/Microsoft.Extensions.AI.Templates/src/ChatWithCustomData/ChatWithCustomData-CSharp.Web/Components/Pages/Chat/Chat.razor
index a7b1502d894..8aa0ec9fd28 100644
--- a/src/ProjectTemplates/Microsoft.Extensions.AI.Templates/src/ChatWithCustomData/ChatWithCustomData-CSharp.Web/Components/Pages/Chat/Chat.razor
+++ b/src/ProjectTemplates/Microsoft.Extensions.AI.Templates/src/ChatWithCustomData/ChatWithCustomData-CSharp.Web/Components/Pages/Chat/Chat.razor
@@ -40,6 +40,7 @@
         Don't refer to the presence of citations; just emit these tags right at the end, with no surrounding text.
         ";
 
+    private int statefulMessageCount;
     private readonly ChatOptions chatOptions = new();
     private readonly List<ChatMessage> messages = new();
     private CancellationTokenSource? currentResponseCancellation;
@@ -49,6 +50,7 @@
 
     protected override void OnInitialized()
     {
+        statefulMessageCount = 0;
         messages.Add(new(ChatRole.System, SystemPrompt));
         chatOptions.Tools = [AIFunctionFactory.Create(SearchAsync)];
     }
@@ -66,15 +68,17 @@
         var responseText = new TextContent("");
         currentResponseMessage = new ChatMessage(ChatRole.Assistant, [responseText]);
         currentResponseCancellation = new();
-        await foreach (var update in ChatClient.GetStreamingResponseAsync([.. messages], chatOptions, currentResponseCancellation.Token))
+        await foreach (var update in ChatClient.GetStreamingResponseAsync(messages.Skip(statefulMessageCount), chatOptions, currentResponseCancellation.Token))
         {
             messages.AddMessages(update, filter: c => c is not TextContent);
             responseText.Text += update.Text;
+            chatOptions.ConversationId = update.ConversationId;
             ChatMessageItem.NotifyChanged(currentResponseMessage);
         }
 
         // Store the final response in the conversation, and begin getting suggestions
         messages.Add(currentResponseMessage!);
+        statefulMessageCount = chatOptions.ConversationId is not null ? messages.Count : 0;
         currentResponseMessage = null;
         chatSuggestions?.Update(messages);
     }
@@ -96,6 +100,8 @@
         CancelAnyCurrentResponse();
         messages.Clear();
         messages.Add(new(ChatRole.System, SystemPrompt));
+        chatOptions.ConversationId = null;
+        statefulMessageCount = 0;
         chatSuggestions?.Clear();
         await chatInput!.FocusAsync();
     }
diff --git a/src/ProjectTemplates/Microsoft.Extensions.AI.Templates/src/ChatWithCustomData/ChatWithCustomData-CSharp.Web/Program.cs b/src/ProjectTemplates/Microsoft.Extensions.AI.Templates/src/ChatWithCustomData/ChatWithCustomData-CSharp.Web/Program.cs
index f3f5740066f..f8d2826ab9a 100644
--- a/src/ProjectTemplates/Microsoft.Extensions.AI.Templates/src/ChatWithCustomData/ChatWithCustomData-CSharp.Web/Program.cs
+++ b/src/ProjectTemplates/Microsoft.Extensions.AI.Templates/src/ChatWithCustomData/ChatWithCustomData-CSharp.Web/Program.cs
@@ -47,7 +47,9 @@
 //   dotnet user-secrets set OpenAI:Key YOUR-API-KEY
 var openAIClient = new OpenAIClient(
     new ApiKeyCredential(builder.Configuration["OpenAI:Key"] ?? throw new InvalidOperationException("Missing configuration: OpenAI:Key. See the README for details.")));
-var chatClient = openAIClient.GetChatClient("gpt-4o-mini").AsIChatClient();
+#pragma warning disable OPENAI001 // Type is for evaluation purposes only and is subject to change or removal in future updates. Suppress this diagnostic to proceed.
+var chatClient = openAIClient.GetOpenAIResponseClient("gpt-4o-mini").AsIChatClient();
+#pragma warning restore OPENAI001 // Type is for evaluation purposes only and is subject to change or removal in future updates. Suppress this diagnostic to proceed.
 var embeddingGenerator = openAIClient.GetEmbeddingClient("text-embedding-3-small").AsIEmbeddingGenerator();
 #elif (IsAzureAiFoundry)
 
@@ -66,7 +68,9 @@
 #else
     new ApiKeyCredential(builder.Configuration["AzureOpenAI:Key"] ?? throw new InvalidOperationException("Missing configuration: AzureOpenAi:Key. See the README for details.")));
 #endif
-var chatClient = azureOpenAi.GetChatClient("gpt-4o-mini").AsIChatClient();
+#pragma warning disable OPENAI001 // Type is for evaluation purposes only and is subject to change or removal in future updates. Suppress this diagnostic to proceed.
+var chatClient = azureOpenAi.GetOpenAIResponseClient("gpt-4o-mini").AsIChatClient();
+#pragma warning restore OPENAI001 // Type is for evaluation purposes only and is subject to change or removal in future updates. Suppress this diagnostic to proceed.
 var embeddingGenerator = azureOpenAi.GetEmbeddingClient("text-embedding-3-small").AsIEmbeddingGenerator();
 #endif
 
diff --git a/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.AzureOpenAI_Qdrant_Aspire.verified/aichatweb/aichatweb.Web/Components/Pages/Chat/Chat.razor b/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.AzureOpenAI_Qdrant_Aspire.verified/aichatweb/aichatweb.Web/Components/Pages/Chat/Chat.razor
index a7b1502d894..8aa0ec9fd28 100644
--- a/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.AzureOpenAI_Qdrant_Aspire.verified/aichatweb/aichatweb.Web/Components/Pages/Chat/Chat.razor
+++ b/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.AzureOpenAI_Qdrant_Aspire.verified/aichatweb/aichatweb.Web/Components/Pages/Chat/Chat.razor
@@ -40,6 +40,7 @@
         Don't refer to the presence of citations; just emit these tags right at the end, with no surrounding text.
         ";
 
+    private int statefulMessageCount;
     private readonly ChatOptions chatOptions = new();
     private readonly List<ChatMessage> messages = new();
     private CancellationTokenSource? currentResponseCancellation;
@@ -49,6 +50,7 @@
 
     protected override void OnInitialized()
     {
+        statefulMessageCount = 0;
         messages.Add(new(ChatRole.System, SystemPrompt));
         chatOptions.Tools = [AIFunctionFactory.Create(SearchAsync)];
     }
@@ -66,15 +68,17 @@
         var responseText = new TextContent("");
         currentResponseMessage = new ChatMessage(ChatRole.Assistant, [responseText]);
         currentResponseCancellation = new();
-        await foreach (var update in ChatClient.GetStreamingResponseAsync([.. messages], chatOptions, currentResponseCancellation.Token))
+        await foreach (var update in ChatClient.GetStreamingResponseAsync(messages.Skip(statefulMessageCount), chatOptions, currentResponseCancellation.Token))
         {
             messages.AddMessages(update, filter: c => c is not TextContent);
             responseText.Text += update.Text;
+            chatOptions.ConversationId = update.ConversationId;
             ChatMessageItem.NotifyChanged(currentResponseMessage);
         }
 
         // Store the final response in the conversation, and begin getting suggestions
         messages.Add(currentResponseMessage!);
+        statefulMessageCount = chatOptions.ConversationId is not null ? messages.Count : 0;
         currentResponseMessage = null;
         chatSuggestions?.Update(messages);
     }
@@ -96,6 +100,8 @@
         CancelAnyCurrentResponse();
         messages.Clear();
         messages.Add(new(ChatRole.System, SystemPrompt));
+        chatOptions.ConversationId = null;
+        statefulMessageCount = 0;
         chatSuggestions?.Clear();
         await chatInput!.FocusAsync();
     }
diff --git a/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.Basic.verified/aichatweb/Components/Pages/Chat/Chat.razor b/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.Basic.verified/aichatweb/Components/Pages/Chat/Chat.razor
index a7b1502d894..8aa0ec9fd28 100644
--- a/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.Basic.verified/aichatweb/Components/Pages/Chat/Chat.razor
+++ b/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.Basic.verified/aichatweb/Components/Pages/Chat/Chat.razor
@@ -40,6 +40,7 @@
         Don't refer to the presence of citations; just emit these tags right at the end, with no surrounding text.
         ";
 
+    private int statefulMessageCount;
     private readonly ChatOptions chatOptions = new();
     private readonly List<ChatMessage> messages = new();
     private CancellationTokenSource? currentResponseCancellation;
@@ -49,6 +50,7 @@
 
     protected override void OnInitialized()
     {
+        statefulMessageCount = 0;
         messages.Add(new(ChatRole.System, SystemPrompt));
         chatOptions.Tools = [AIFunctionFactory.Create(SearchAsync)];
     }
@@ -66,15 +68,17 @@
         var responseText = new TextContent("");
         currentResponseMessage = new ChatMessage(ChatRole.Assistant, [responseText]);
         currentResponseCancellation = new();
-        await foreach (var update in ChatClient.GetStreamingResponseAsync([.. messages], chatOptions, currentResponseCancellation.Token))
+        await foreach (var update in ChatClient.GetStreamingResponseAsync(messages.Skip(statefulMessageCount), chatOptions, currentResponseCancellation.Token))
         {
             messages.AddMessages(update, filter: c => c is not TextContent);
             responseText.Text += update.Text;
+            chatOptions.ConversationId = update.ConversationId;
             ChatMessageItem.NotifyChanged(currentResponseMessage);
         }
 
         // Store the final response in the conversation, and begin getting suggestions
         messages.Add(currentResponseMessage!);
+        statefulMessageCount = chatOptions.ConversationId is not null ? messages.Count : 0;
         currentResponseMessage = null;
         chatSuggestions?.Update(messages);
     }
@@ -96,6 +100,8 @@
         CancelAnyCurrentResponse();
         messages.Clear();
         messages.Add(new(ChatRole.System, SystemPrompt));
+        chatOptions.ConversationId = null;
+        statefulMessageCount = 0;
         chatSuggestions?.Clear();
         await chatInput!.FocusAsync();
     }
diff --git a/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.BasicAspire.verified/aichatweb/aichatweb.Web/Components/Pages/Chat/Chat.razor b/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.BasicAspire.verified/aichatweb/aichatweb.Web/Components/Pages/Chat/Chat.razor
index a7b1502d894..8aa0ec9fd28 100644
--- a/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.BasicAspire.verified/aichatweb/aichatweb.Web/Components/Pages/Chat/Chat.razor
+++ b/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.BasicAspire.verified/aichatweb/aichatweb.Web/Components/Pages/Chat/Chat.razor
@@ -40,6 +40,7 @@
         Don't refer to the presence of citations; just emit these tags right at the end, with no surrounding text.
         ";
 
+    private int statefulMessageCount;
     private readonly ChatOptions chatOptions = new();
     private readonly List<ChatMessage> messages = new();
     private CancellationTokenSource? currentResponseCancellation;
@@ -49,6 +50,7 @@
 
     protected override void OnInitialized()
     {
+        statefulMessageCount = 0;
         messages.Add(new(ChatRole.System, SystemPrompt));
         chatOptions.Tools = [AIFunctionFactory.Create(SearchAsync)];
     }
@@ -66,15 +68,17 @@
         var responseText = new TextContent("");
         currentResponseMessage = new ChatMessage(ChatRole.Assistant, [responseText]);
         currentResponseCancellation = new();
-        await foreach (var update in ChatClient.GetStreamingResponseAsync([.. messages], chatOptions, currentResponseCancellation.Token))
+        await foreach (var update in ChatClient.GetStreamingResponseAsync(messages.Skip(statefulMessageCount), chatOptions, currentResponseCancellation.Token))
         {
             messages.AddMessages(update, filter: c => c is not TextContent);
             responseText.Text += update.Text;
+            chatOptions.ConversationId = update.ConversationId;
             ChatMessageItem.NotifyChanged(currentResponseMessage);
         }
 
         // Store the final response in the conversation, and begin getting suggestions
         messages.Add(currentResponseMessage!);
+        statefulMessageCount = chatOptions.ConversationId is not null ? messages.Count : 0;
         currentResponseMessage = null;
         chatSuggestions?.Update(messages);
     }
@@ -96,6 +100,8 @@
         CancelAnyCurrentResponse();
         messages.Clear();
         messages.Add(new(ChatRole.System, SystemPrompt));
+        chatOptions.ConversationId = null;
+        statefulMessageCount = 0;
         chatSuggestions?.Clear();
         await chatInput!.FocusAsync();
     }
diff --git a/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.Ollama_Qdrant.verified/aichatweb/aichatweb.Web/Components/Pages/Chat/Chat.razor b/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.Ollama_Qdrant.verified/aichatweb/aichatweb.Web/Components/Pages/Chat/Chat.razor
index a7b1502d894..8aa0ec9fd28 100644
--- a/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.Ollama_Qdrant.verified/aichatweb/aichatweb.Web/Components/Pages/Chat/Chat.razor
+++ b/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.Ollama_Qdrant.verified/aichatweb/aichatweb.Web/Components/Pages/Chat/Chat.razor
@@ -40,6 +40,7 @@
         Don't refer to the presence of citations; just emit these tags right at the end, with no surrounding text.
         ";
 
+    private int statefulMessageCount;
     private readonly ChatOptions chatOptions = new();
     private readonly List<ChatMessage> messages = new();
     private CancellationTokenSource? currentResponseCancellation;
@@ -49,6 +50,7 @@
 
     protected override void OnInitialized()
     {
+        statefulMessageCount = 0;
         messages.Add(new(ChatRole.System, SystemPrompt));
         chatOptions.Tools = [AIFunctionFactory.Create(SearchAsync)];
     }
@@ -66,15 +68,17 @@
         var responseText = new TextContent("");
         currentResponseMessage = new ChatMessage(ChatRole.Assistant, [responseText]);
         currentResponseCancellation = new();
-        await foreach (var update in ChatClient.GetStreamingResponseAsync([.. messages], chatOptions, currentResponseCancellation.Token))
+        await foreach (var update in ChatClient.GetStreamingResponseAsync(messages.Skip(statefulMessageCount), chatOptions, currentResponseCancellation.Token))
         {
             messages.AddMessages(update, filter: c => c is not TextContent);
             responseText.Text += update.Text;
+            chatOptions.ConversationId = update.ConversationId;
             ChatMessageItem.NotifyChanged(currentResponseMessage);
         }
 
         // Store the final response in the conversation, and begin getting suggestions
         messages.Add(currentResponseMessage!);
+        statefulMessageCount = chatOptions.ConversationId is not null ? messages.Count : 0;
         currentResponseMessage = null;
         chatSuggestions?.Update(messages);
     }
@@ -96,6 +100,8 @@
         CancelAnyCurrentResponse();
         messages.Clear();
         messages.Add(new(ChatRole.System, SystemPrompt));
+        chatOptions.ConversationId = null;
+        statefulMessageCount = 0;
         chatSuggestions?.Clear();
         await chatInput!.FocusAsync();
     }
diff --git a/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.OpenAI_AzureAISearch.verified/aichatweb/Components/Pages/Chat/Chat.razor b/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.OpenAI_AzureAISearch.verified/aichatweb/Components/Pages/Chat/Chat.razor
index a7b1502d894..8aa0ec9fd28 100644
--- a/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.OpenAI_AzureAISearch.verified/aichatweb/Components/Pages/Chat/Chat.razor
+++ b/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.OpenAI_AzureAISearch.verified/aichatweb/Components/Pages/Chat/Chat.razor
@@ -40,6 +40,7 @@
         Don't refer to the presence of citations; just emit these tags right at the end, with no surrounding text.
         ";
 
+    private int statefulMessageCount;
     private readonly ChatOptions chatOptions = new();
     private readonly List<ChatMessage> messages = new();
     private CancellationTokenSource? currentResponseCancellation;
@@ -49,6 +50,7 @@
 
     protected override void OnInitialized()
     {
+        statefulMessageCount = 0;
         messages.Add(new(ChatRole.System, SystemPrompt));
         chatOptions.Tools = [AIFunctionFactory.Create(SearchAsync)];
     }
@@ -66,15 +68,17 @@
         var responseText = new TextContent("");
         currentResponseMessage = new ChatMessage(ChatRole.Assistant, [responseText]);
         currentResponseCancellation = new();
-        await foreach (var update in ChatClient.GetStreamingResponseAsync([.. messages], chatOptions, currentResponseCancellation.Token))
+        await foreach (var update in ChatClient.GetStreamingResponseAsync(messages.Skip(statefulMessageCount), chatOptions, currentResponseCancellation.Token))
         {
             messages.AddMessages(update, filter: c => c is not TextContent);
             responseText.Text += update.Text;
+            chatOptions.ConversationId = update.ConversationId;
             ChatMessageItem.NotifyChanged(currentResponseMessage);
         }
 
         // Store the final response in the conversation, and begin getting suggestions
         messages.Add(currentResponseMessage!);
+        statefulMessageCount = chatOptions.ConversationId is not null ? messages.Count : 0;
         currentResponseMessage = null;
         chatSuggestions?.Update(messages);
     }
@@ -96,6 +100,8 @@
         CancelAnyCurrentResponse();
         messages.Clear();
         messages.Add(new(ChatRole.System, SystemPrompt));
+        chatOptions.ConversationId = null;
+        statefulMessageCount = 0;
         chatSuggestions?.Clear();
         await chatInput!.FocusAsync();
     }
diff --git a/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.OpenAI_AzureAISearch.verified/aichatweb/Program.cs b/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.OpenAI_AzureAISearch.verified/aichatweb/Program.cs
index 2b9f0790817..d469d9c43db 100644
--- a/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.OpenAI_AzureAISearch.verified/aichatweb/Program.cs
+++ b/test/ProjectTemplates/Microsoft.Extensions.AI.Templates.IntegrationTests/Snapshots/aichatweb.OpenAI_AzureAISearch.verified/aichatweb/Program.cs
@@ -16,7 +16,9 @@
 //   dotnet user-secrets set OpenAI:Key YOUR-API-KEY
 var openAIClient = new OpenAIClient(
     new ApiKeyCredential(builder.Configuration["OpenAI:Key"] ?? throw new InvalidOperationException("Missing configuration: OpenAI:Key. See the README for details.")));
-var chatClient = openAIClient.GetChatClient("gpt-4o-mini").AsIChatClient();
+#pragma warning disable OPENAI001 // Type is for evaluation purposes only and is subject to change or removal in future updates. Suppress this diagnostic to proceed.
+var chatClient = openAIClient.GetOpenAIResponseClient("gpt-4o-mini").AsIChatClient();
+#pragma warning restore OPENAI001 // Type is for evaluation purposes only and is subject to change or removal in future updates. Suppress this diagnostic to proceed.
 var embeddingGenerator = openAIClient.GetEmbeddingClient("text-embedding-3-small").AsIEmbeddingGenerator();
 
 // You will need to set the endpoint and key to your own values