diff --git a/dotnet/src/Microsoft.Agents.AI/ChatClient/ChatClientAgent.cs b/dotnet/src/Microsoft.Agents.AI/ChatClient/ChatClientAgent.cs
index 1133e10a8a..c43f90155f 100644
--- a/dotnet/src/Microsoft.Agents.AI/ChatClient/ChatClientAgent.cs
+++ b/dotnet/src/Microsoft.Agents.AI/ChatClient/ChatClientAgent.cs
@@ -476,7 +476,7 @@ internal async Task NotifyProvidersOfNewMessagesAsync(
         ChatOptions? chatOptions,
         CancellationToken cancellationToken)
     {
-        ChatHistoryProvider? chatHistoryProvider = this.ResolveChatHistoryProvider(chatOptions);
+        ChatHistoryProvider? chatHistoryProvider = this.ResolveChatHistoryProvider(session, chatOptions);
 
         if (chatHistoryProvider is not null)
         {
@@ -508,7 +508,7 @@ internal async Task NotifyProvidersOfFailureAsync(
         ChatOptions? chatOptions,
         CancellationToken cancellationToken)
     {
-        ChatHistoryProvider? chatHistoryProvider = this.ResolveChatHistoryProvider(chatOptions);
+        ChatHistoryProvider? chatHistoryProvider = this.ResolveChatHistoryProvider(session, chatOptions);
 
         if (chatHistoryProvider is not null)
         {
@@ -974,14 +974,17 @@ private void WarnOnMissingPerServiceCallChatHistoryPersistingChatClient()
         }
     }
 
-    private ChatHistoryProvider? ResolveChatHistoryProvider(ChatOptions? chatOptions)
+    private ChatHistoryProvider? ResolveChatHistoryProvider(ChatClientAgentSession session, ChatOptions? chatOptions)
     {
-        ChatHistoryProvider? provider = chatOptions?.ConversationId is null ? this.ChatHistoryProvider : null;
+        bool serviceStoresHistory = !this.RequiresPerServiceCallChatHistoryPersistence
+            && (!string.IsNullOrWhiteSpace(session.ConversationId)
+                || !string.IsNullOrWhiteSpace(chatOptions?.ConversationId));
+        ChatHistoryProvider? provider = serviceStoresHistory ? null : this.ChatHistoryProvider;
 
         // If someone provided an override ChatHistoryProvider via AdditionalProperties, we should use that instead.
         if (chatOptions?.AdditionalProperties?.TryGetValue(out ChatHistoryProvider? overrideProvider) is true)
         {
-            if (this._agentOptions?.ThrowOnChatHistoryProviderConflict is true && string.IsNullOrWhiteSpace(chatOptions?.ConversationId) is false)
+            if (this._agentOptions?.ThrowOnChatHistoryProviderConflict is true && serviceStoresHistory)
             {
                 throw new InvalidOperationException(
                     $"Only {nameof(ChatClientAgentSession.ConversationId)} or {nameof(this.ChatHistoryProvider)} may be used, but not both. The current {nameof(ChatClientAgentSession)} has a {nameof(ChatClientAgentSession.ConversationId)} indicating server-side chat history management, but an override {nameof(this.ChatHistoryProvider)} was provided via {nameof(AgentRunOptions.AdditionalProperties)}.");
@@ -1019,7 +1022,7 @@ internal async Task<IEnumerable<ChatMessage>> LoadChatHistoryAsync(
         ChatOptions? chatOptions,
         CancellationToken cancellationToken)
     {
-        var chatHistoryProvider = this.ResolveChatHistoryProvider(chatOptions);
+        var chatHistoryProvider = this.ResolveChatHistoryProvider(session, chatOptions);
         if (chatHistoryProvider is null)
         {
             return messages;
diff --git a/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgent_ChatHistoryManagementTests.cs b/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgent_ChatHistoryManagementTests.cs
index 410ee4edda..eff8f3d83d 100644
--- a/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgent_ChatHistoryManagementTests.cs
+++ b/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgent_ChatHistoryManagementTests.cs
@@ -385,11 +385,11 @@ public async Task RunAsync_Throws_WhenThrowEnabledRegardlessOfClearSettingAsync(
     }
 
     /// <summary>
-    /// Verify that RunAsync does not throw when no ChatHistoryProvider is configured on options,
-    /// even if the service returns a conversation id (default InMemoryChatHistoryProvider is used but not from options).
+    /// Verify that RunAsync does not persist to the default InMemoryChatHistoryProvider when
+    /// the service returns a conversation id.
     /// </summary>
     [Fact]
-    public async Task RunAsync_DoesNotThrow_WhenNoChatHistoryProviderInOptionsAndConversationIdReturnedAsync()
+    public async Task RunAsync_DoesNotUseDefaultInMemoryChatHistoryProvider_WhenConversationIdReturnedAsync()
     {
         // Arrange
         Mock<IChatClient> mockService = new();
@@ -407,8 +407,10 @@ public async Task RunAsync_DoesNotThrow_WhenNoChatHistoryProviderInOptionsAndCon
         ChatClientAgentSession? session = await agent.CreateSessionAsync() as ChatClientAgentSession;
         await agent.RunAsync([new(ChatRole.User, "test")], session);
 
-        // Assert - no exception, session gets the conversation id
+        // Assert
         Assert.Equal("ConvId", session!.ConversationId);
+        var inMemoryProvider = Assert.IsType<InMemoryChatHistoryProvider>(agent.ChatHistoryProvider);
+        Assert.Empty(inMemoryProvider.GetMessages(session));
     }
 
     #endregion