diff --git a/apps/server/src/terminal/Layers/Manager.test.ts b/apps/server/src/terminal/Layers/Manager.test.ts
index 304b49d42b79..0d45bfcb294b 100644
--- a/apps/server/src/terminal/Layers/Manager.test.ts
+++ b/apps/server/src/terminal/Layers/Manager.test.ts
@@ -394,6 +394,21 @@ describe("TerminalManager", () => {
     manager.dispose();
   });
 
+  it("ignores trailing writes after terminal exit", async () => {
+    const { manager, ptyAdapter } = makeManager();
+    await manager.open(openInput());
+    const process = ptyAdapter.processes[0];
+    expect(process).toBeDefined();
+    if (!process) return;
+
+    process.emitExit({ exitCode: 0, signal: 0 });
+
+    await expect(manager.write({ threadId: "thread-1", data: "\r" })).resolves.toBeUndefined();
+    expect(process.writes).toEqual([]);
+
+    manager.dispose();
+  });
+
   it("emits subprocess activity events when child-process state changes", async () => {
     let hasRunningSubprocess = false;
     const { manager } = makeManager(5, {
diff --git a/apps/server/src/terminal/Layers/Manager.ts b/apps/server/src/terminal/Layers/Manager.ts
index fa766da570f1..a0e4ad705ccf 100644
--- a/apps/server/src/terminal/Layers/Manager.ts
+++ b/apps/server/src/terminal/Layers/Manager.ts
@@ -438,6 +438,9 @@ export class TerminalManagerRuntime extends EventEmitter<TerminalManagerEvents>
     const input = decodeTerminalWriteInput(raw);
     const session = this.requireSession(input.threadId, input.terminalId);
     if (!session.process || session.status !== "running") {
+      if (session.status === "exited") {
+        return;
+      }
       throw new Error(
         `Terminal is not running for thread: ${input.threadId}, terminal: ${input.terminalId}`,
       );
diff --git a/apps/web/src/components/ThreadTerminalDrawer.tsx b/apps/web/src/components/ThreadTerminalDrawer.tsx
index ab86780487a8..c2653a90dada 100644
--- a/apps/web/src/components/ThreadTerminalDrawer.tsx
+++ b/apps/web/src/components/ThreadTerminalDrawer.tsx
@@ -112,6 +112,7 @@ interface TerminalViewportProps {
   terminalId: string;
   cwd: string;
   runtimeEnv?: Record<string, string>;
+  onSessionExited: () => void;
   focusRequestId: number;
   autoFocus: boolean;
   resizeEpoch: number;
@@ -123,6 +124,7 @@ function TerminalViewport({
   terminalId,
   cwd,
   runtimeEnv,
+  onSessionExited,
   focusRequestId,
   autoFocus,
   resizeEpoch,
@@ -131,6 +133,12 @@ function TerminalViewport({
   const containerRef = useRef<HTMLDivElement>(null);
   const terminalRef = useRef<Terminal | null>(null);
   const fitAddonRef = useRef<FitAddon | null>(null);
+  const onSessionExitedRef = useRef(onSessionExited);
+  const hasHandledExitRef = useRef(false);
+
+  useEffect(() => {
+    onSessionExitedRef.current = onSessionExited;
+  }, [onSessionExited]);
 
   useEffect(() => {
     const mount = containerRef.current;
@@ -306,6 +314,7 @@ function TerminalViewport({
       }
 
       if (event.type === "started" || event.type === "restarted") {
+        hasHandledExitRef.current = false;
         activeTerminal.write("\u001bc");
         if (event.snapshot.history.length > 0) {
           activeTerminal.write(event.snapshot.history);
@@ -335,6 +344,16 @@ function TerminalViewport({
           activeTerminal,
           details.length > 0 ? `Process exited (${details})` : "Process exited",
         );
+        if (hasHandledExitRef.current) {
+          return;
+        }
+        hasHandledExitRef.current = true;
+        window.setTimeout(() => {
+          if (!hasHandledExitRef.current) {
+            return;
+          }
+          onSessionExitedRef.current();
+        }, 0);
       }
     });
 
@@ -783,6 +802,7 @@ export default function ThreadTerminalDrawer({
                         terminalId={terminalId}
                         cwd={cwd}
                         {...(runtimeEnv ? { runtimeEnv } : {})}
+                        onSessionExited={() => onCloseTerminal(terminalId)}
                         focusRequestId={focusRequestId}
                         autoFocus={terminalId === resolvedActiveTerminalId}
                         resizeEpoch={resizeEpoch}
@@ -800,6 +820,7 @@ export default function ThreadTerminalDrawer({
                   terminalId={resolvedActiveTerminalId}
                   cwd={cwd}
                   {...(runtimeEnv ? { runtimeEnv } : {})}
+                  onSessionExited={() => onCloseTerminal(resolvedActiveTerminalId)}
                   focusRequestId={focusRequestId}
                   autoFocus
                   resizeEpoch={resizeEpoch}