diff --git a/dotnet/src/Microsoft.Agents.AI/ChatClient/ChatClientAgent.cs b/dotnet/src/Microsoft.Agents.AI/ChatClient/ChatClientAgent.cs
index d04d9bb9fb..049322785c 100644
--- a/dotnet/src/Microsoft.Agents.AI/ChatClient/ChatClientAgent.cs
+++ b/dotnet/src/Microsoft.Agents.AI/ChatClient/ChatClientAgent.cs
@@ -289,6 +289,7 @@ public sealed partial class ChatClientAgent : AIAgent
     public override AgentThread GetNewThread()
         => new ChatClientAgentThread
         {
+            MessageStore = this._agentOptions?.ChatMessageStoreFactory?.Invoke(new() { SerializedState = default, JsonSerializerOptions = null }),
             AIContextProvider = this._agentOptions?.AIContextProviderFactory?.Invoke(new() { SerializedState = default, JsonSerializerOptions = null })
         };
 
@@ -316,6 +317,34 @@ public sealed partial class ChatClientAgent : AIAgent
             AIContextProvider = this._agentOptions?.AIContextProviderFactory?.Invoke(new() { SerializedState = default, JsonSerializerOptions = null })
         };
 
+    /// <summary>
+    /// Creates a new agent thread instance using an existing <see cref="ChatMessageStore"/> to continue a conversation.
+    /// </summary>
+    /// <param name="chatMessageStore">The <see cref="ChatMessageStore"/> instance to use for managing the conversation's message history.</param>
+    /// <returns>
+    /// A new <see cref="AgentThread"/> instance configured to work with the provided <paramref name="chatMessageStore"/>.
+    /// </returns>
+    /// <remarks>
+    /// <para>
+    /// This method creates threads that do not support server-side conversation storage.
+    /// Some AI services require server-side conversation storage to function properly, and creating a thread
+    /// with a <see cref="ChatMessageStore"/> may not be compatible with these services.
+    /// </para>
+    /// <para>
+    /// Where a service requires server-side conversation storage, use <see cref="GetNewThread(string)"/>.
+    /// </para>
+    /// <para>
+    /// If the agent detects, during the first run, that the underlying AI service requires server-side conversation storage,
+    /// the thread will throw an exception to indicate that it cannot continue using the provided <see cref="ChatMessageStore"/>.
+    /// </para>
+    /// </remarks>
+    public AgentThread GetNewThread(ChatMessageStore chatMessageStore)
+        => new ChatClientAgentThread()
+        {
+            MessageStore = Throw.IfNull(chatMessageStore),
+            AIContextProvider = this._agentOptions?.AIContextProviderFactory?.Invoke(new() { SerializedState = default, JsonSerializerOptions = null })
+        };
+
     /// <inheritdoc/>
     public override AgentThread DeserializeThread(JsonElement serializedThread, JsonSerializerOptions? jsonSerializerOptions = null)
     {
diff --git a/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgentTests.cs b/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgentTests.cs
index e9d458aba4..920f9f82ee 100644
--- a/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgentTests.cs
+++ b/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgentTests.cs
@@ -459,10 +459,74 @@ public partial class ChatClientAgentTests
     }
 
     /// <summary>
-    /// Verify that RunAsync doesn't use the ChatMessageStore factory when the chat client returns a conversation id.
+    /// Verify that RunAsync uses the default InMemoryChatMessageStore when the chat client returns no conversation id.
     /// </summary>
     [Fact]
-    public async Task RunAsyncIgnoresChatMessageStoreWhenConversationIdReturnedByChatClientAsync()
+    public async Task RunAsyncUsesDefaultInMemoryChatMessageStoreWhenNoConversationIdReturnedByChatClientAsync()
+    {
+        // Arrange
+        Mock<IChatClient> mockService = new();
+        mockService.Setup(
+            s => s.GetResponseAsync(
+                It.IsAny<IEnumerable<ChatMessage>>(),
+                It.IsAny<ChatOptions>(),
+                It.IsAny<CancellationToken>())).ReturnsAsync(new ChatResponse([new(ChatRole.Assistant, "response")]));
+        ChatClientAgent agent = new(mockService.Object, options: new()
+        {
+            Instructions = "test instructions",
+        });
+
+        // Act
+        ChatClientAgentThread? thread = agent.GetNewThread() as ChatClientAgentThread;
+        await agent.RunAsync([new(ChatRole.User, "test")], thread);
+
+        // Assert
+        var messageStore = Assert.IsType<InMemoryChatMessageStore>(thread!.MessageStore);
+        Assert.Equal(2, messageStore.Count);
+        Assert.Equal("test", messageStore[0].Text);
+        Assert.Equal("response", messageStore[1].Text);
+    }
+
+    /// <summary>
+    /// Verify that RunAsync uses the ChatMessageStore factory when the chat client returns no conversation id.
+    /// </summary>
+    [Fact]
+    public async Task RunAsyncUsesChatMessageStoreFactoryWhenProvidedAndNoConversationIdReturnedByChatClientAsync()
+    {
+        // Arrange
+        Mock<IChatClient> mockService = new();
+        mockService.Setup(
+            s => s.GetResponseAsync(
+                It.IsAny<IEnumerable<ChatMessage>>(),
+                It.IsAny<ChatOptions>(),
+                It.IsAny<CancellationToken>())).ReturnsAsync(new ChatResponse([new(ChatRole.Assistant, "response")]));
+
+        Mock<ChatMessageStore> mockChatMessageStore = new();
+
+        Mock<Func<ChatClientAgentOptions.ChatMessageStoreFactoryContext, ChatMessageStore>> mockFactory = new();
+        mockFactory.Setup(f => f(It.IsAny<ChatClientAgentOptions.ChatMessageStoreFactoryContext>())).Returns(mockChatMessageStore.Object);
+
+        ChatClientAgent agent = new(mockService.Object, options: new()
+        {
+            Instructions = "test instructions",
+            ChatMessageStoreFactory = mockFactory.Object
+        });
+
+        // Act
+        ChatClientAgentThread? thread = agent.GetNewThread() as ChatClientAgentThread;
+        await agent.RunAsync([new(ChatRole.User, "test")], thread);
+
+        // Assert
+        Assert.IsType<ChatMessageStore>(thread!.MessageStore, exactMatch: false);
+        mockChatMessageStore.Verify(s => s.AddMessagesAsync(It.Is<IEnumerable<ChatMessage>>(x => x.Count() == 2), It.IsAny<CancellationToken>()), Times.Once);
+        mockFactory.Verify(f => f(It.IsAny<ChatClientAgentOptions.ChatMessageStoreFactoryContext>()), Times.Once);
+    }
+
+    /// <summary>
+    /// Verify that RunAsync throws when a ChatMessageStore Factory is provided and the chat client returns a conversation id.
+    /// </summary>
+    [Fact]
+    public async Task RunAsyncThrowsWhenChatMessageStoreFactoryProvidedAndConversationIdReturnedByChatClientAsync()
     {
         // Arrange
         Mock<IChatClient> mockService = new();
@@ -479,13 +543,10 @@ public partial class ChatClientAgentTests
             ChatMessageStoreFactory = mockFactory.Object
         });
 
-        // Act
+        // Act & Assert
         ChatClientAgentThread? thread = agent.GetNewThread() as ChatClientAgentThread;
-        await agent.RunAsync([new(ChatRole.User, "test")], thread);
-
-        // Assert
-        Assert.Equal("ConvId", thread!.ConversationId);
-        mockFactory.Verify(f => f(It.IsAny<ChatClientAgentOptions.ChatMessageStoreFactoryContext>()), Times.Never);
+        var exception = await Assert.ThrowsAsync<InvalidOperationException>(() => agent.RunAsync([new(ChatRole.User, "test")], thread));
+        Assert.Equal("Only the ConversationId or MessageStore may be set, but not both and switching from one to another is not supported.", exception.Message);
     }
 
     /// <summary>
@@ -1914,10 +1975,10 @@ public partial class ChatClientAgentTests
     }
 
     /// <summary>
-    /// Verify that RunStreamingAsync doesn't use the ChatMessageStore factory when the chat client returns a conversation id.
+    /// Verify that RunStreamingAsync throws when a ChatMessageStore factory is provided and the chat client returns a conversation id.
     /// </summary>
     [Fact]
-    public async Task RunStreamingAsyncIgnoresChatMessageStoreWhenConversationIdReturnedByChatClientAsync()
+    public async Task RunStreamingAsyncThrowsWhenChatMessageStoreFactoryProvidedAndConversationIdReturnedByChatClientAsync()
     {
         // Arrange
         Mock<IChatClient> mockService = new();
@@ -1939,13 +2000,10 @@ public partial class ChatClientAgentTests
             ChatMessageStoreFactory = mockFactory.Object
         });
 
-        // Act
+        // Act & Assert
         ChatClientAgentThread? thread = agent.GetNewThread() as ChatClientAgentThread;
-        await agent.RunStreamingAsync([new(ChatRole.User, "test")], thread).ToListAsync();
-
-        // Assert
-        Assert.Equal("ConvId", thread!.ConversationId);
-        mockFactory.Verify(f => f(It.IsAny<ChatClientAgentOptions.ChatMessageStoreFactoryContext>()), Times.Never);
+        var exception = await Assert.ThrowsAsync<InvalidOperationException>(async () => await agent.RunStreamingAsync([new(ChatRole.User, "test")], thread).ToListAsync());
+        Assert.Equal("Only the ConversationId or MessageStore may be set, but not both and switching from one to another is not supported.", exception.Message);
     }
 
     /// <summary>
@@ -2074,37 +2132,6 @@ public partial class ChatClientAgentTests
 
     #endregion
 
-    #region GetNewThread Tests
-
-    [Fact]
-    public void GetNewThreadUsesAIContextProviderFactoryIfProvided()
-    {
-        // Arrange
-        var mockChatClient = new Mock<IChatClient>();
-        var mockContextProvider = new Mock<AIContextProvider>();
-        var factoryCalled = false;
-        var agent = new ChatClientAgent(mockChatClient.Object, new ChatClientAgentOptions
-        {
-            Instructions = "Test instructions",
-            AIContextProviderFactory = _ =>
-            {
-                factoryCalled = true;
-                return mockContextProvider.Object;
-            }
-        });
-
-        // Act
-        var thread = agent.GetNewThread();
-
-        // Assert
-        Assert.True(factoryCalled, "AIContextProviderFactory was not called.");
-        Assert.IsType<ChatClientAgentThread>(thread);
-        var typedThread = (ChatClientAgentThread)thread;
-        Assert.Same(mockContextProvider.Object, typedThread.AIContextProvider);
-    }
-
-    #endregion
-
     #region Background Responses Tests
 
     [Theory]
diff --git a/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgent_DeserializeThreadTests.cs b/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgent_DeserializeThreadTests.cs
new file mode 100644
index 0000000000..1fd9a71b98
--- /dev/null
+++ b/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgent_DeserializeThreadTests.cs
@@ -0,0 +1,79 @@
+// Copyright (c) Microsoft. All rights reserved.
+
+using System.Text.Json;
+using Microsoft.Extensions.AI;
+using Moq;
+
+namespace Microsoft.Agents.AI.UnitTests.ChatClient;
+
+/// <summary>
+/// Contains unit tests for the ChatClientAgent.DeserializeThread methods.
+/// </summary>
+public class ChatClientAgent_DeserializeThreadTests
+{
+    [Fact]
+    public void DeserializeThread_UsesAIContextProviderFactory_IfProvided()
+    {
+        // Arrange
+        var mockChatClient = new Mock<IChatClient>();
+        var mockContextProvider = new Mock<AIContextProvider>();
+        var factoryCalled = false;
+        var agent = new ChatClientAgent(mockChatClient.Object, new ChatClientAgentOptions
+        {
+            Instructions = "Test instructions",
+            AIContextProviderFactory = _ =>
+            {
+                factoryCalled = true;
+                return mockContextProvider.Object;
+            }
+        });
+
+        var json = JsonSerializer.Deserialize("""
+            {
+                "aiContextProviderState": ["CP1"]
+            }
+            """, TestJsonSerializerContext.Default.JsonElement);
+
+        // Act
+        var thread = agent.DeserializeThread(json);
+
+        // Assert
+        Assert.True(factoryCalled, "AIContextProviderFactory was not called.");
+        Assert.IsType<ChatClientAgentThread>(thread);
+        var typedThread = (ChatClientAgentThread)thread;
+        Assert.Same(mockContextProvider.Object, typedThread.AIContextProvider);
+    }
+
+    [Fact]
+    public void DeserializeThread_UsesChatMessageStoreFactory_IfProvided()
+    {
+        // Arrange
+        var mockChatClient = new Mock<IChatClient>();
+        var mockMessageStore = new Mock<ChatMessageStore>();
+        var factoryCalled = false;
+        var agent = new ChatClientAgent(mockChatClient.Object, new ChatClientAgentOptions
+        {
+            Instructions = "Test instructions",
+            ChatMessageStoreFactory = _ =>
+            {
+                factoryCalled = true;
+                return mockMessageStore.Object;
+            }
+        });
+
+        var json = JsonSerializer.Deserialize("""
+            {
+                "storeState": { }
+            }
+            """, TestJsonSerializerContext.Default.JsonElement);
+
+        // Act
+        var thread = agent.DeserializeThread(json);
+
+        // Assert
+        Assert.True(factoryCalled, "ChatMessageStoreFactory was not called.");
+        Assert.IsType<ChatClientAgentThread>(thread);
+        var typedThread = (ChatClientAgentThread)thread;
+        Assert.Same(mockMessageStore.Object, typedThread.MessageStore);
+    }
+}
diff --git a/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgent_GetNewThreadTests.cs b/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgent_GetNewThreadTests.cs
new file mode 100644
index 0000000000..43e0bef8bc
--- /dev/null
+++ b/dotnet/tests/Microsoft.Agents.AI.UnitTests/ChatClient/ChatClientAgent_GetNewThreadTests.cs
@@ -0,0 +1,100 @@
+// Copyright (c) Microsoft. All rights reserved.
+
+using Microsoft.Extensions.AI;
+using Moq;
+
+namespace Microsoft.Agents.AI.UnitTests.ChatClient;
+
+/// <summary>
+/// Contains unit tests for the ChatClientAgent.GetNewThread methods.
+/// </summary>
+public class ChatClientAgent_GetNewThreadTests
+{
+    [Fact]
+    public void GetNewThread_UsesAIContextProviderFactory_IfProvided()
+    {
+        // Arrange
+        var mockChatClient = new Mock<IChatClient>();
+        var mockContextProvider = new Mock<AIContextProvider>();
+        var factoryCalled = false;
+        var agent = new ChatClientAgent(mockChatClient.Object, new ChatClientAgentOptions
+        {
+            Instructions = "Test instructions",
+            AIContextProviderFactory = _ =>
+            {
+                factoryCalled = true;
+                return mockContextProvider.Object;
+            }
+        });
+
+        // Act
+        var thread = agent.GetNewThread();
+
+        // Assert
+        Assert.True(factoryCalled, "AIContextProviderFactory was not called.");
+        Assert.IsType<ChatClientAgentThread>(thread);
+        var typedThread = (ChatClientAgentThread)thread;
+        Assert.Same(mockContextProvider.Object, typedThread.AIContextProvider);
+    }
+
+    [Fact]
+    public void GetNewThread_UsesChatMessageStoreFactory_IfProvided()
+    {
+        // Arrange
+        var mockChatClient = new Mock<IChatClient>();
+        var mockMessageStore = new Mock<ChatMessageStore>();
+        var factoryCalled = false;
+        var agent = new ChatClientAgent(mockChatClient.Object, new ChatClientAgentOptions
+        {
+            Instructions = "Test instructions",
+            ChatMessageStoreFactory = _ =>
+            {
+                factoryCalled = true;
+                return mockMessageStore.Object;
+            }
+        });
+
+        // Act
+        var thread = agent.GetNewThread();
+
+        // Assert
+        Assert.True(factoryCalled, "ChatMessageStoreFactory was not called.");
+        Assert.IsType<ChatClientAgentThread>(thread);
+        var typedThread = (ChatClientAgentThread)thread;
+        Assert.Same(mockMessageStore.Object, typedThread.MessageStore);
+    }
+
+    [Fact]
+    public void GetNewThread_UsesChatMessageStore_FromTypedOverload()
+    {
+        // Arrange
+        var mockChatClient = new Mock<IChatClient>();
+        var mockMessageStore = new Mock<ChatMessageStore>();
+        var agent = new ChatClientAgent(mockChatClient.Object);
+
+        // Act
+        var thread = agent.GetNewThread(mockMessageStore.Object);
+
+        // Assert
+        Assert.IsType<ChatClientAgentThread>(thread);
+        var typedThread = (ChatClientAgentThread)thread;
+        Assert.Same(mockMessageStore.Object, typedThread.MessageStore);
+    }
+
+    [Fact]
+    public void GetNewThread_UsesConversationId_FromTypedOverload()
+    {
+        // Arrange
+        var mockChatClient = new Mock<IChatClient>();
+        const string TestConversationId = "test_conversation_id";
+        var agent = new ChatClientAgent(mockChatClient.Object);
+
+        // Act
+        var thread = agent.GetNewThread(TestConversationId);
+
+        // Assert
+        Assert.IsType<ChatClientAgentThread>(thread);
+        var typedThread = (ChatClientAgentThread)thread;
+        Assert.Equal(TestConversationId, typedThread.ConversationId);
+    }
+}