diff --git a/dotnet/src/Microsoft.Agents.AI.A2A/A2AAgent.cs b/dotnet/src/Microsoft.Agents.AI.A2A/A2AAgent.cs
index e4491970ad..887e780104 100644
--- a/dotnet/src/Microsoft.Agents.AI.A2A/A2AAgent.cs
+++ b/dotnet/src/Microsoft.Agents.AI.A2A/A2AAgent.cs
@@ -75,11 +75,7 @@ internal sealed class A2AAgent : AIAgent
     {
         _ = Throw.IfNull(messages);
 
-        thread ??= this.GetNewThread();
-        if (thread is not A2AAgentThread typedThread)
-        {
-            throw new InvalidOperationException("The provided thread is not compatible with the agent. Only threads created by the agent can be used.");
-        }
+        A2AAgentThread typedThread = this.GetA2AThread(thread, options);
 
         this._logger.LogA2AAgentInvokingAgent(nameof(RunAsync), this.Id, this.Name);
 
@@ -142,11 +138,7 @@ internal sealed class A2AAgent : AIAgent
     {
         _ = Throw.IfNull(messages);
 
-        thread ??= this.GetNewThread();
-        if (thread is not A2AAgentThread typedThread)
-        {
-            throw new InvalidOperationException("The provided thread is not compatible with the agent. Only threads created by the agent can be used.");
-        }
+        A2AAgentThread typedThread = this.GetA2AThread(thread, options);
 
         this._logger.LogA2AAgentInvokingAgent(nameof(RunStreamingAsync), this.Id, this.Name);
 
@@ -217,6 +209,26 @@ internal sealed class A2AAgent : AIAgent
     /// <inheritdoc/>
     public override string? Description => this._description ?? base.Description;
 
+    private A2AAgentThread GetA2AThread(AgentThread? thread, AgentRunOptions? options)
+    {
+        // Aligning with other agent implementations that support background responses, where
+        // a thread is required for background responses to prevent inconsistent experience
+        // for callers if they forget to provide the thread for initial or follow-up runs.
+        if (options?.AllowBackgroundResponses is true && thread is null)
+        {
+            throw new InvalidOperationException("A thread must be provided when AllowBackgroundResponses is enabled.");
+        }
+
+        thread ??= this.GetNewThread();
+
+        if (thread is not A2AAgentThread typedThread)
+        {
+            throw new InvalidOperationException($"The provided thread type {thread.GetType()} is not compatible with the agent. Only A2A agent created threads are supported.");
+        }
+
+        return typedThread;
+    }
+
     private static void UpdateThread(A2AAgentThread? thread, string? contextId, string? taskId = null)
     {
         if (thread is null)
diff --git a/dotnet/tests/Microsoft.Agents.AI.A2A.UnitTests/A2AAgentTests.cs b/dotnet/tests/Microsoft.Agents.AI.A2A.UnitTests/A2AAgentTests.cs
index 05c7f5ba08..f079fc5ed8 100644
--- a/dotnet/tests/Microsoft.Agents.AI.A2A.UnitTests/A2AAgentTests.cs
+++ b/dotnet/tests/Microsoft.Agents.AI.A2A.UnitTests/A2AAgentTests.cs
@@ -799,12 +799,80 @@ public sealed class A2AAgentTests : IDisposable
         Assert.Equal(TaskId, a2aThread.TaskId);
     }
 
+    [Fact]
+    public async Task RunAsync_WithAllowBackgroundResponsesAndNoThread_ThrowsInvalidOperationExceptionAsync()
+    {
+        // Arrange
+        var inputMessages = new List<ChatMessage>
+        {
+            new(ChatRole.User, "Test message")
+        };
+
+        var options = new AgentRunOptions { AllowBackgroundResponses = true };
+
+        // Act & Assert
+        await Assert.ThrowsAsync<InvalidOperationException>(() => this._agent.RunAsync(inputMessages, null, options));
+    }
+
+    [Fact]
+    public async Task RunStreamingAsync_WithAllowBackgroundResponsesAndNoThread_ThrowsInvalidOperationExceptionAsync()
+    {
+        // Arrange
+        var inputMessages = new List<ChatMessage>
+        {
+            new(ChatRole.User, "Test message")
+        };
+
+        var options = new AgentRunOptions { AllowBackgroundResponses = true };
+
+        // Act & Assert
+        await Assert.ThrowsAsync<InvalidOperationException>(async () =>
+        {
+            await foreach (var _ in this._agent.RunStreamingAsync(inputMessages, null, options))
+            {
+                // Just iterate through to trigger the exception
+            }
+        });
+    }
+
+    [Fact]
+    public async Task RunAsync_WithInvalidThreadType_ThrowsInvalidOperationExceptionAsync()
+    {
+        // Arrange
+        // Create a thread from a different agent type
+        var invalidThread = new CustomAgentThread();
+
+        // Act & Assert
+        await Assert.ThrowsAsync<InvalidOperationException>(() => this._agent.RunAsync(invalidThread));
+    }
+
+    [Fact]
+    public async Task RunStreamingAsync_WithInvalidThreadType_ThrowsInvalidOperationExceptionAsync()
+    {
+        // Arrange
+        var inputMessages = new List<ChatMessage>
+        {
+            new(ChatRole.User, "Test message")
+        };
+
+        // Create a thread from a different agent type
+        var invalidThread = new CustomAgentThread();
+
+        // Act & Assert
+        await Assert.ThrowsAsync<InvalidOperationException>(async () => await this._agent.RunStreamingAsync(inputMessages, invalidThread).ToListAsync());
+    }
+
     public void Dispose()
     {
         this._handler.Dispose();
         this._httpClient.Dispose();
     }
 
+    /// <summary>
+    /// Custom agent thread class for testing invalid thread type scenario.
+    /// </summary>
+    private sealed class CustomAgentThread : AgentThread;
+
     internal sealed class A2AClientHttpMessageHandlerStub : HttpMessageHandler
     {
         public JsonRpcRequest? CapturedJsonRpcRequest { get; set; }