diff --git a/multimodal/tarko/agent-interface/src/agent-event-stream.ts b/multimodal/tarko/agent-interface/src/agent-event-stream.ts
index f8d37a00ad..b51a515893 100644
--- a/multimodal/tarko/agent-interface/src/agent-event-stream.ts
+++ b/multimodal/tarko/agent-interface/src/agent-event-stream.ts
@@ -385,6 +385,13 @@ export namespace AgentEventStream {
     type: 'codebase';
   }
 
+  /**
+   * User interrupt metadata
+   */
+  export interface UserInterruptMetadata extends BaseEnvironmentInputMetadata {
+    type: 'user_interrupt';
+  }
+
   /**
    * Generic metadata for other types
    */
@@ -399,6 +406,7 @@ export namespace AgentEventStream {
     | ScreenshotMetadata
     | TextMetadata
     | CodebaseMetadata
+    | UserInterruptMetadata
     | GenericMetadata;
 
   /**
diff --git a/multimodal/tarko/agent-server/src/api/controllers/queries.ts b/multimodal/tarko/agent-server/src/api/controllers/queries.ts
index 464b2572f9..390e771788 100644
--- a/multimodal/tarko/agent-server/src/api/controllers/queries.ts
+++ b/multimodal/tarko/agent-server/src/api/controllers/queries.ts
@@ -43,6 +43,23 @@ export async function executeQuery(req: Request, res: Response) {
   }
 
   try {
+    // Check if agent is currently running
+    const session = req.session!;
+    const isAgentRunning = session.getProcessingStatus();
+
+    if (isAgentRunning) {
+      // Agent is running - insert as environment input instead of starting new query
+      await session.insertEnvironmentInput(query, 'User interrupt message during agent execution');
+      
+      // Return success response for environment input insertion
+      return res.status(200).json({ 
+        success: true, 
+        type: 'environment_input_inserted',
+        message: 'User input inserted as environment input during agent execution'
+      });
+    }
+
+    // Agent is not running - proceed with normal query
     // Get server instance to access workspace path
     const server = req.app.locals.server;
     const workspacePath = server.getCurrentWorkspace();
@@ -71,7 +88,7 @@ export async function executeQuery(req: Request, res: Response) {
     };
 
     // Use enhanced error handling in runQuery with environment input
-    const response = await req.session!.runQuery(runOptions);
+    const response = await session.runQuery(runOptions);
 
     if (response.success) {
       res.status(200).json({ result: response.result });
@@ -97,6 +114,23 @@ export async function executeStreamingQuery(req: Request, res: Response) {
   }
 
   try {
+    // Check if agent is currently running
+    const session = req.session!;
+    const isAgentRunning = session.getProcessingStatus();
+
+    if (isAgentRunning) {
+      // Agent is running - insert as environment input instead of starting new query
+      await session.insertEnvironmentInput(query, 'User interrupt message during agent execution');
+      
+      // Return success response for environment input insertion
+      return res.status(200).json({ 
+        success: true, 
+        type: 'environment_input_inserted',
+        message: 'User input inserted as environment input during agent execution'
+      });
+    }
+
+    // Agent is not running - proceed with normal streaming query
     // Set response headers for streaming
     res.setHeader('Content-Type', 'text/event-stream');
     res.setHeader('Cache-Control', 'no-cache');
@@ -130,7 +164,7 @@ export async function executeStreamingQuery(req: Request, res: Response) {
     };
 
     // Get streaming response with environment input - any errors will be returned as events
-    const eventStream = await req.session!.runQueryStreaming(runOptions);
+    const eventStream = await session.runQueryStreaming(runOptions);
 
     // Stream events one by one
     for await (const event of eventStream) {
diff --git a/multimodal/tarko/agent-server/src/core/AgentSession.ts b/multimodal/tarko/agent-server/src/core/AgentSession.ts
index a3f5f50368..eb38dd31c2 100644
--- a/multimodal/tarko/agent-server/src/core/AgentSession.ts
+++ b/multimodal/tarko/agent-server/src/core/AgentSession.ts
@@ -504,6 +504,51 @@ export class AgentSession {
     }
   }
 
+  /**
+   * Insert environment input while agent is running
+   * @param content Environment input content
+   * @param description Optional description of the input
+   * @returns Promise resolving when environment input is inserted
+   */
+  async insertEnvironmentInput(
+    content: string | ChatCompletionContentPart[],
+    description?: string,
+  ): Promise<void> {
+    try {
+      // Create environment input event
+      const environmentInputEvent = this.agent.getEventStream().createEvent('environment_input', {
+        content,
+        description: description || 'User interrupt message during agent execution',
+        metadata: {
+          type: 'user_interrupt',
+        },
+      });
+
+      // Process the event through our handler for storage and AGIO
+      const handleEvent = this.createEventHandler();
+      await handleEvent(environmentInputEvent);
+
+      // Emit to client via event bridge
+      this.eventBridge.emit('environment_input', {
+        sessionId: this.id,
+        event: environmentInputEvent,
+      });
+
+      if (this.server.isDebug) {
+        console.log('[DEBUG] Environment input inserted', {
+          sessionId: this.id,
+          contentType: typeof content === 'string' ? 'string' : 'ContentPart',
+          description,
+        });
+      }
+    } catch (error) {
+      this.eventBridge.emit('error', {
+        message: error instanceof Error ? error.message : String(error),
+      });
+      throw error;
+    }
+  }
+
   /**
    * Update session configuration (model and runtime settings)
    * The configuration will be used in subsequent queries
diff --git a/multimodal/tarko/agent-server/tests/api/contextual-references.test.ts b/multimodal/tarko/agent-server/tests/api/contextual-references.test.ts
index e82e20f222..2809772056 100644
--- a/multimodal/tarko/agent-server/tests/api/contextual-references.test.ts
+++ b/multimodal/tarko/agent-server/tests/api/contextual-references.test.ts
@@ -10,7 +10,12 @@ import { Request, Response } from 'express';
 const { mockContextProcessor, mockImageProcessor, mockSession, mockServer } = vi.hoisted(() => ({
   mockContextProcessor: { processContextualReferences: vi.fn() },
   mockImageProcessor: { compressImagesInQuery: vi.fn() },
-  mockSession: { runQuery: vi.fn(), runQueryStreaming: vi.fn() },
+  mockSession: { 
+    runQuery: vi.fn(), 
+    runQueryStreaming: vi.fn(),
+    getProcessingStatus: vi.fn().mockReturnValue(false),
+    insertEnvironmentInput: vi.fn()
+  },
   mockServer: { getCurrentWorkspace: vi.fn().mockReturnValue('/workspace') },
 }));
 
@@ -57,6 +62,8 @@ describe('Contextual References Bug Fix', () => {
   beforeEach(() => {
     vi.clearAllMocks();
     mockImageProcessor.compressImagesInQuery.mockImplementation(q => Promise.resolve(q));
+    // Reset to default: agent not running
+    mockSession.getProcessingStatus.mockReturnValue(false);
   });
 
   describe('environmentInput conditional logic', () => {
diff --git a/multimodal/tarko/agent-server/tests/api/queries.test.ts b/multimodal/tarko/agent-server/tests/api/queries.test.ts
index 9811ac774d..89228c0eff 100644
--- a/multimodal/tarko/agent-server/tests/api/queries.test.ts
+++ b/multimodal/tarko/agent-server/tests/api/queries.test.ts
@@ -10,7 +10,13 @@ import { Request, Response } from 'express';
 const { mockContextProcessor, mockImageProcessor, mockSession, mockServer } = vi.hoisted(() => ({
   mockContextProcessor: { processContextualReferences: vi.fn() },
   mockImageProcessor: { compressImagesInQuery: vi.fn() },
-  mockSession: { runQuery: vi.fn(), runQueryStreaming: vi.fn(), abortQuery: vi.fn() },
+  mockSession: { 
+    runQuery: vi.fn(), 
+    runQueryStreaming: vi.fn(), 
+    abortQuery: vi.fn(),
+    getProcessingStatus: vi.fn().mockReturnValue(false),
+    insertEnvironmentInput: vi.fn()
+  },
   mockServer: { getCurrentWorkspace: vi.fn().mockReturnValue('/test/workspace') },
 }));
 
@@ -53,9 +59,35 @@ const mockProcessing = (expandedContext: string | null, compressedQuery: any = n
 describe('Queries Controller', () => {
   beforeEach(() => {
     vi.clearAllMocks();
+    // Reset to default: agent not running
+    mockSession.getProcessingStatus.mockReturnValue(false);
   });
 
   describe('executeQuery', () => {
+    it('should insert environment input when agent is running', async () => {
+      const userQuery = 'User interrupt message';
+      const req = createRequest(userQuery);
+      const res = createResponse();
+
+      mockSession.getProcessingStatus.mockReturnValue(true);
+      mockSession.insertEnvironmentInput.mockResolvedValue(undefined);
+
+      await executeQuery(req as Request, res as Response);
+
+      expect(mockSession.getProcessingStatus).toHaveBeenCalled();
+      expect(mockSession.insertEnvironmentInput).toHaveBeenCalledWith(
+        userQuery,
+        'User interrupt message during agent execution'
+      );
+      expect(res.status).toHaveBeenCalledWith(200);
+      expect(res.json).toHaveBeenCalledWith({
+        success: true,
+        type: 'environment_input_inserted',
+        message: 'User input inserted as environment input during agent execution'
+      });
+      expect(mockSession.runQuery).not.toHaveBeenCalled();
+    });
+
     it('should process context and pass environmentInput when references exist', async () => {
       const userQuery = 'Test query with @file reference';
       const expandedContext = 'File content: function test() { return true; }';
@@ -164,6 +196,31 @@ describe('Queries Controller', () => {
   });
 
   describe('executeStreamingQuery', () => {
+    it('should insert environment input when agent is running', async () => {
+      const userQuery = 'User interrupt streaming message';
+      const req = createRequest(userQuery);
+      const res = createResponse();
+
+      mockSession.getProcessingStatus.mockReturnValue(true);
+      mockSession.insertEnvironmentInput.mockResolvedValue(undefined);
+
+      await executeStreamingQuery(req as Request, res as Response);
+
+      expect(mockSession.getProcessingStatus).toHaveBeenCalled();
+      expect(mockSession.insertEnvironmentInput).toHaveBeenCalledWith(
+        userQuery,
+        'User interrupt message during agent execution'
+      );
+      expect(res.status).toHaveBeenCalledWith(200);
+      expect(res.json).toHaveBeenCalledWith({
+        success: true,
+        type: 'environment_input_inserted',
+        message: 'User input inserted as environment input during agent execution'
+      });
+      expect(mockSession.runQueryStreaming).not.toHaveBeenCalled();
+      expect(res.setHeader).not.toHaveBeenCalled();
+    });
+
     it('should process context and stream with environmentInput', async () => {
       const userQuery = 'Streaming query with @dir reference';
       const expandedContext = 'Directory listing: file1.js, file2.ts';
diff --git a/multimodal/tarko/agent-ui/src/common/services/apiService.ts b/multimodal/tarko/agent-ui/src/common/services/apiService.ts
index 87cf60a422..6870ba5838 100644
--- a/multimodal/tarko/agent-ui/src/common/services/apiService.ts
+++ b/multimodal/tarko/agent-ui/src/common/services/apiService.ts
@@ -243,6 +243,18 @@ class ApiService {
         throw new Error(`Failed to send query: ${response.statusText}`);
       }
 
+      // Check if response is JSON (environment input insertion) or streaming
+      const contentType = response.headers.get('content-type');
+      if (contentType?.includes('application/json')) {
+        // This is an environment input insertion response
+        const result = await response.json();
+        if (result.type === 'environment_input_inserted') {
+          console.log('User input inserted as environment input during agent execution');
+          return; // No streaming for environment input insertion
+        }
+      }
+
+      // Handle streaming response
       const reader = response.body?.getReader();
       if (!reader) {
         throw new Error('ReadableStream not supported');
diff --git a/multimodal/tarko/agent-ui/src/standalone/chat/ChatPanel.tsx b/multimodal/tarko/agent-ui/src/standalone/chat/ChatPanel.tsx
index 0019a3b6e7..dd27d06f6e 100644
--- a/multimodal/tarko/agent-ui/src/standalone/chat/ChatPanel.tsx
+++ b/multimodal/tarko/agent-ui/src/standalone/chat/ChatPanel.tsx
@@ -88,7 +88,6 @@ export const ChatPanel: React.FC = () => {
             isDisabled={
               !currentSessionId ||
               currentSessionId === 'creating' ||
-              isProcessing ||
               !connectionStatus.connected ||
               isReplayMode
             }
diff --git a/multimodal/tarko/agent-ui/src/standalone/chat/Message/Message.css b/multimodal/tarko/agent-ui/src/standalone/chat/Message/Message.css
index e9769c2aad..190afbbdba 100644
--- a/multimodal/tarko/agent-ui/src/standalone/chat/Message/Message.css
+++ b/multimodal/tarko/agent-ui/src/standalone/chat/Message/Message.css
@@ -90,6 +90,24 @@
   @apply px-2 text-gray-700 dark:text-gray-300 max-w-full mx-auto;
 }
 
+.environment-message-minimal {
+  @apply bg-amber-50 dark:bg-amber-900/20 border border-amber-200 dark:border-amber-800/50 text-amber-800 dark:text-amber-200 px-4 py-3 rounded-lg mx-auto max-w-fit text-sm;
+  position: relative;
+}
+
+.environment-message-minimal::before {
+  content: '💬';
+  @apply mr-2 opacity-70;
+}
+
+.environment-message-minimal .prose {
+  @apply text-amber-800 dark:text-amber-200 m-0;
+}
+
+.environment-message-minimal .prose p {
+  @apply m-0 text-amber-800 dark:text-amber-200;
+}
+
 .message-gap {
   margin-bottom: 1rem;
   position: relative;
diff --git a/multimodal/tarko/agent-ui/src/standalone/chat/Message/components/MessageGroup.tsx b/multimodal/tarko/agent-ui/src/standalone/chat/Message/components/MessageGroup.tsx
index 634bacdd9c..bb053d0afa 100644
--- a/multimodal/tarko/agent-ui/src/standalone/chat/Message/components/MessageGroup.tsx
+++ b/multimodal/tarko/agent-ui/src/standalone/chat/Message/components/MessageGroup.tsx
@@ -24,16 +24,17 @@ interface MessageGroupProps {
 export const MessageGroup: React.FC<MessageGroupProps> = ({ messages, isThinking }) => {
   const isProcessing = useAtomValue(isProcessingAtom);
 
-  // Filter out environment messages
-  const filteredMessages = messages.filter((msg) => msg.role !== 'environment');
+  // Keep all messages including environment messages
+  const filteredMessages = messages;
 
   // If no messages after filtering, render nothing
   if (filteredMessages.length === 0) {
     return null;
   }
 
-  // Get user messages and assistant messages
+  // Get user messages, environment messages, and assistant messages
   const userMessages = filteredMessages.filter((msg) => msg.role === 'user');
+  const environmentMessages = filteredMessages.filter((msg) => msg.role === 'environment');
   const assistantMessages = filteredMessages.filter(
     (msg) => msg.role === 'assistant' || msg.role === 'system',
   );
@@ -76,6 +77,11 @@ export const MessageGroup: React.FC<MessageGroupProps> = ({ messages, isThinking
         return <Message key={userMsg.id} message={userMsg} />;
       })}
 
+      {/* Render environment messages (inserted messages) */}
+      {environmentMessages.map((envMsg) => (
+        <Message key={envMsg.id} message={envMsg} />
+      ))}
+
       {/* Render all assistant messages - each message renders independently, supporting streaming display */}
       {assistantMessages.map((message, index) => (
         <Message
diff --git a/multimodal/tarko/agent-ui/src/standalone/chat/MessageInput/ChatInput.tsx b/multimodal/tarko/agent-ui/src/standalone/chat/MessageInput/ChatInput.tsx
index 70c4d5cd43..b61499babc 100644
--- a/multimodal/tarko/agent-ui/src/standalone/chat/MessageInput/ChatInput.tsx
+++ b/multimodal/tarko/agent-ui/src/standalone/chat/MessageInput/ChatInput.tsx
@@ -380,7 +380,7 @@ export const ChatInput: React.FC<ChatInputProps> = ({
     connectionStatus && !connectionStatus.connected
       ? 'Server disconnected...'
       : isProcessing
-        ? `${getAgentTitle()} is running...`
+        ? `Insert a message while ${getAgentTitle()} is running... (Ctrl+Enter to send)`
         : contextualSelectorEnabled
           ? `Ask ${getAgentTitle()} something... (Use @ to reference files/folders, Ctrl+Enter to send)`
           : `Ask ${getAgentTitle()} something... (Ctrl+Enter to send)`;
@@ -532,64 +532,78 @@ export const ChatInput: React.FC<ChatInputProps> = ({
             )}
 
             {/* Action buttons */}
-            <AnimatePresence mode="wait">
-              {connectionStatus && !connectionStatus.connected ? (
-                <motion.button
-                  key="reconnect-btn"
-                  initial={{ opacity: 0, scale: 0.8 }}
-                  animate={{ opacity: 1, scale: 1 }}
-                  exit={{ opacity: 0, scale: 0.8 }}
-                  type="button"
-                  onClick={onReconnect}
-                  className="absolute right-3 bottom-3 p-2 rounded-full text-gray-500 hover:bg-gray-50 dark:hover:bg-gray-700/30 dark:text-gray-400 transition-all duration-200 hover:scale-105 active:scale-90"
-                  title="Try to reconnect"
-                >
-                  <FiRefreshCw
-                    size={20}
-                    className={connectionStatus.reconnecting ? 'animate-spin' : ''}
-                  />
-                </motion.button>
-              ) : isProcessing ? (
-                <motion.button
-                  key="abort-btn"
-                  initial={{ opacity: 0 }}
-                  animate={{ opacity: 1 }}
-                  exit={{ opacity: 0 }}
-                  transition={{ duration: 0.2 }}
-                  type="button"
-                  onClick={handleAbort}
-                  disabled={isAborting}
-                  className={`absolute right-3 bottom-3 w-10 h-10 rounded-full flex items-center justify-center transition-all duration-200 hover:scale-105 active:scale-95 ${
-                    isAborting
-                      ? 'bg-gradient-to-r from-indigo-100 via-purple-100 to-pink-100 dark:from-indigo-800/30 dark:via-purple-800/30 dark:to-pink-800/30 text-indigo-400 dark:text-indigo-500 cursor-not-allowed border-2 border-indigo-200 dark:border-indigo-700/50'
-                      : 'bg-gradient-to-r from-indigo-50 via-purple-50 to-pink-50 hover:from-indigo-100 hover:via-purple-100 hover:to-pink-100 dark:from-indigo-900/20 dark:via-purple-900/20 dark:to-pink-900/20 dark:hover:from-indigo-900/30 dark:hover:via-purple-900/30 dark:hover:to-pink-900/30 text-indigo-600 dark:text-indigo-400 border-2 border-indigo-200 dark:border-indigo-700/50'
-                  } shadow-sm bg-[length:200%_200%] animate-border-flow`}
-                  title="Stop generation"
-                >
-                  {isAborting ? (
-                    <div className="w-4 h-4 border-2 border-current border-t-transparent rounded-full animate-spin" />
-                  ) : (
-                    <div className="w-3 h-3 bg-current rounded-sm" />
-                  )}
-                </motion.button>
-              ) : (
-                <motion.button
-                  key="send-btn"
-                  initial={{ opacity: 0, scale: 0.8 }}
-                  animate={{ opacity: 1, scale: 1 }}
-                  exit={{ opacity: 0, scale: 0.8 }}
-                  type="submit"
-                  disabled={isMessageEmpty(contextualState.input, uploadedImages) || isDisabled}
-                  className={`absolute right-3 bottom-3 p-3 rounded-full transition-all duration-200 hover:scale-105 active:scale-90 ${
-                    isMessageEmpty(contextualState.input, uploadedImages) || isDisabled
-                      ? 'bg-gray-100 dark:bg-gray-700 text-gray-400 cursor-not-allowed'
-                      : 'bg-gradient-to-r from-indigo-500 to-purple-500 dark:from-indigo-400 dark:via-purple-400 dark:to-pink-400 text-white dark:text-gray-900 shadow-sm'
-                  }`}
-                >
-                  <FiSend size={18} />
-                </motion.button>
-              )}
-            </AnimatePresence>
+            <div className="absolute right-3 bottom-3 flex items-center gap-2">
+              {/* Reconnect button */}
+              <AnimatePresence>
+                {connectionStatus && !connectionStatus.connected && (
+                  <motion.button
+                    key="reconnect-btn"
+                    initial={{ opacity: 0, scale: 0.8 }}
+                    animate={{ opacity: 1, scale: 1 }}
+                    exit={{ opacity: 0, scale: 0.8 }}
+                    type="button"
+                    onClick={onReconnect}
+                    className="p-2 rounded-full text-gray-500 hover:bg-gray-50 dark:hover:bg-gray-700/30 dark:text-gray-400 transition-all duration-200 hover:scale-105 active:scale-90"
+                    title="Try to reconnect"
+                  >
+                    <FiRefreshCw
+                      size={20}
+                      className={connectionStatus.reconnecting ? 'animate-spin' : ''}
+                    />
+                  </motion.button>
+                )}
+              </AnimatePresence>
+
+              {/* Abort button - show when processing */}
+              <AnimatePresence>
+                {isProcessing && (
+                  <motion.button
+                    key="abort-btn"
+                    initial={{ opacity: 0, scale: 0.8 }}
+                    animate={{ opacity: 1, scale: 1 }}
+                    exit={{ opacity: 0, scale: 0.8 }}
+                    transition={{ duration: 0.2 }}
+                    type="button"
+                    onClick={handleAbort}
+                    disabled={isAborting}
+                    className={`w-10 h-10 rounded-full flex items-center justify-center transition-all duration-200 hover:scale-105 active:scale-95 ${
+                      isAborting
+                        ? 'bg-gradient-to-r from-indigo-100 via-purple-100 to-pink-100 dark:from-indigo-800/30 dark:via-purple-800/30 dark:to-pink-800/30 text-indigo-400 dark:text-indigo-500 cursor-not-allowed border-2 border-indigo-200 dark:border-indigo-700/50'
+                        : 'bg-gradient-to-r from-indigo-50 via-purple-50 to-pink-50 hover:from-indigo-100 hover:via-purple-100 hover:to-pink-100 dark:from-indigo-900/20 dark:via-purple-900/20 dark:to-pink-900/20 dark:hover:from-indigo-900/30 dark:hover:via-purple-900/30 dark:hover:to-pink-900/30 text-indigo-600 dark:text-indigo-400 border-2 border-indigo-200 dark:border-indigo-700/50'
+                    } shadow-sm bg-[length:200%_200%] animate-border-flow`}
+                    title="Stop generation"
+                  >
+                    {isAborting ? (
+                      <div className="w-4 h-4 border-2 border-current border-t-transparent rounded-full animate-spin" />
+                    ) : (
+                      <div className="w-3 h-3 bg-current rounded-sm" />
+                    )}
+                  </motion.button>
+                )}
+              </AnimatePresence>
+
+              {/* Send button - always show when not reconnecting */}
+              <AnimatePresence>
+                {!(connectionStatus && !connectionStatus.connected) && (
+                  <motion.button
+                    key="send-btn"
+                    initial={{ opacity: 0, scale: 0.8 }}
+                    animate={{ opacity: 1, scale: 1 }}
+                    exit={{ opacity: 0, scale: 0.8 }}
+                    type="submit"
+                    disabled={isMessageEmpty(contextualState.input, uploadedImages) || isDisabled}
+                    className={`p-3 rounded-full transition-all duration-200 hover:scale-105 active:scale-90 ${
+                      isMessageEmpty(contextualState.input, uploadedImages) || isDisabled
+                        ? 'bg-gray-100 dark:bg-gray-700 text-gray-400 cursor-not-allowed'
+                        : 'bg-gradient-to-r from-indigo-500 to-purple-500 dark:from-indigo-400 dark:via-purple-400 dark:to-pink-400 text-white dark:text-gray-900 shadow-sm'
+                    }`}
+                    title={isProcessing ? 'Insert message' : 'Send message'}
+                  >
+                    <FiSend size={18} />
+                  </motion.button>
+                )}
+              </AnimatePresence>
+            </div>
           </div>
         </div>
       </form>