diff --git a/extensions/memory-core/src/memory/manager-sync-ops.ts b/extensions/memory-core/src/memory/manager-sync-ops.ts
index f32d52aba3d..ca0881f4713 100644
--- a/extensions/memory-core/src/memory/manager-sync-ops.ts
+++ b/extensions/memory-core/src/memory/manager-sync-ops.ts
@@ -446,6 +446,12 @@ export abstract class MemoryManagerSyncOps {
     this.watcher.on("change", markDirty);
     this.watcher.on("unlink", markDirty);
     this.watcher.on("unlinkDir", markDirty);
+    this.watcher.on("error", (err) => {
+      // File watcher errors (e.g., ENOSPC) should not crash the gateway.
+      // Log the error and continue - memory search still works without auto-sync.
+      const message = err instanceof Error ? err.message : String(err);
+      log.warn(`memory watcher error: ${message}`);
+    });
   }
 
   protected ensureSessionListener() {
diff --git a/src/infra/unhandled-rejections.test.ts b/src/infra/unhandled-rejections.test.ts
index c3731d89b5b..fbe5bcc02db 100644
--- a/src/infra/unhandled-rejections.test.ts
+++ b/src/infra/unhandled-rejections.test.ts
@@ -2,6 +2,7 @@ import { describe, expect, it } from "vitest";
 import {
   isAbortError,
   isBenignUncaughtExceptionError,
+  isTransientFileWatchError,
   isTransientNetworkError,
   isTransientSqliteError,
   isTransientUnhandledRejectionError,
@@ -258,6 +259,87 @@ describe("isTransientSqliteError", () => {
   });
 });
 
+describe("isTransientFileWatchError", () => {
+  it("returns true for ENOSPC with inotify message", () => {
+    const error = Object.assign(new Error("inotify watches exhausted"), { code: "ENOSPC" });
+    expect(isTransientFileWatchError(error)).toBe(true);
+  });
+
+  it("returns true for ENOSPC with file watcher message", () => {
+    const error = Object.assign(new Error("System limit for number of file watchers reached"), {
+      code: "ENOSPC",
+    });
+    expect(isTransientFileWatchError(error)).toBe(true);
+  });
+
+  it("returns true for ENOSPC with watcher error message", () => {
+    const error = Object.assign(new Error("watcher error: ENOSPC"), { code: "ENOSPC" });
+    expect(isTransientFileWatchError(error)).toBe(true);
+  });
+
+  it("returns false for ENOSPC without watch indicator (general disk full)", () => {
+    const error = Object.assign(new Error("write failed: no space left on device"), {
+      code: "ENOSPC",
+    });
+    expect(isTransientFileWatchError(error)).toBe(false);
+  });
+
+  it("returns false for ENOSPC with only 'disk full' message", () => {
+    const error = Object.assign(new Error("ENOSPC: disk full"), { code: "ENOSPC" });
+    expect(isTransientFileWatchError(error)).toBe(false);
+  });
+
+  it("returns true for 'no space left on device' message with watcher context", () => {
+    const error = new Error("file watcher: no space left on device");
+    expect(isTransientFileWatchError(error)).toBe(true);
+  });
+
+  it("returns true for inotify-related error messages", () => {
+    expect(isTransientFileWatchError(new Error("inotify watches exhausted"))).toBe(true);
+    expect(
+      isTransientFileWatchError(new Error("System limit for number of file watchers reached")),
+    ).toBe(true);
+  });
+
+  it("returns true for watcher-related error messages", () => {
+    expect(isTransientFileWatchError(new Error("watcher error: ENOSPC"))).toBe(true);
+    expect(isTransientFileWatchError(new Error("file watcher failed"))).toBe(true);
+  });
+
+  it("returns true for ENOSPC with cause chain containing watch indicator", () => {
+    const cause = Object.assign(new Error("inotify watches exhausted"), { code: "ENOSPC" });
+    const error = Object.assign(new Error("watcher failed"), { cause });
+    expect(isTransientFileWatchError(error)).toBe(true);
+  });
+
+  it("returns false for 'watchdog timeout' (unrelated watch error)", () => {
+    expect(isTransientFileWatchError(new Error("watchdog timeout"))).toBe(false);
+    expect(isTransientFileWatchError(new Error("cannot watch process"))).toBe(false);
+  });
+
+  it("returns false for regular errors without file watch indicators", () => {
+    expect(isTransientFileWatchError(new Error("Something went wrong"))).toBe(false);
+    expect(isTransientFileWatchError(new TypeError("Cannot read property"))).toBe(false);
+    expect(isTransientFileWatchError(new RangeError("Invalid array length"))).toBe(false);
+  });
+
+  it("returns false for other disk errors without ENOSPC", () => {
+    expect(isTransientFileWatchError(new Error("disk quota exceeded"))).toBe(false);
+    expect(
+      isTransientFileWatchError(
+        Object.assign(new Error("read only file system"), { code: "EROFS" }),
+      ),
+    ).toBe(false);
+  });
+
+  it.each([null, undefined, "string error", 42, { message: "plain object" }])(
+    "returns false for non-file-watch input %#",
+    (value) => {
+      expect(isTransientFileWatchError(value)).toBe(false);
+    },
+  );
+});
+
 describe("isTransientUnhandledRejectionError", () => {
   it("treats raw pre-connect network uncaught exceptions as benign", () => {
     const epipe = Object.assign(new Error("write EPIPE"), { code: "EPIPE" });
@@ -287,4 +369,21 @@ describe("isTransientUnhandledRejectionError", () => {
 
     expect(isTransientUnhandledRejectionError(error)).toBe(true);
   });
+
+  it("returns true for transient file watcher errors (ENOSPC + inotify)", () => {
+    const error = Object.assign(new Error("inotify watches exhausted"), { code: "ENOSPC" });
+    expect(isTransientUnhandledRejectionError(error)).toBe(true);
+  });
+
+  it("returns true for file watcher errors with message only", () => {
+    const error = new Error("System limit for number of file watchers reached");
+    expect(isTransientUnhandledRejectionError(error)).toBe(true);
+  });
+
+  it("returns false for ENOSPC without watch indicator (general disk full)", () => {
+    const error = Object.assign(new Error("write failed: no space left on device"), {
+      code: "ENOSPC",
+    });
+    expect(isTransientUnhandledRejectionError(error)).toBe(false);
+  });
 });
diff --git a/src/infra/unhandled-rejections.ts b/src/infra/unhandled-rejections.ts
index 81f57a05af3..ec1e0800bc5 100644
--- a/src/infra/unhandled-rejections.ts
+++ b/src/infra/unhandled-rejections.ts
@@ -350,8 +350,70 @@ export function isTransientSqliteError(err: unknown): boolean {
   return false;
 }
 
+/**
+ * Checks if an error is a transient file watcher error that shouldn't crash the gateway.
+ * These are typically resource exhaustion issues (e.g., inotify watches exhausted) that
+ * can be recovered from by degrading to manual sync mode.
+ *
+ * Note: ENOSPC is a general POSIX error code (disk full, write failures, etc.).
+ * To avoid misclassifying unrelated storage failures, we require both the ENOSPC code
+ * AND a watch/inotify-related message indicator, similar to how hasSqliteSignal gates
+ * SQLite errors.
+ */
+export function isTransientFileWatchError(err: unknown): boolean {
+  if (!err) {
+    return false;
+  }
+
+  for (const candidate of collectNestedUnhandledErrorCandidates(err)) {
+    // Skip non-object candidates early
+    if (!candidate || typeof candidate !== "object") {
+      continue;
+    }
+
+    const code = extractErrorCodeOrErrno(candidate);
+    const rawMessage =
+      "message" in candidate && typeof candidate.message === "string" ? candidate.message : "";
+    const message = normalizeLowercaseStringOrEmpty(rawMessage);
+
+    // ENOSPC requires both the code AND a watch/inotify message indicator
+    // to avoid misclassifying general disk-full errors as transient watcher errors.
+    if (code === "ENOSPC") {
+      if (
+        message.includes("inotify") ||
+        message.includes("watcher") ||
+        message.includes("file watcher") ||
+        message.includes("watch limit") ||
+        message.includes("max watches")
+      ) {
+        return true;
+      }
+      // ENOSPC without watch indicator is not classified here
+      continue;
+    }
+
+    // Check for file watcher error message patterns (without ENOSPC code)
+    if (!message) {
+      continue;
+    }
+    if (
+      message.includes("no space left on device") ||
+      message.includes("enosp") ||
+      message.includes("inotify watches") ||
+      message.includes("file watcher") ||
+      message.includes("watcher error")
+    ) {
+      return true;
+    }
+  }
+
+  return false;
+}
+
 export function isTransientUnhandledRejectionError(err: unknown): boolean {
-  return isTransientNetworkError(err) || isTransientSqliteError(err);
+  return (
+    isTransientNetworkError(err) || isTransientSqliteError(err) || isTransientFileWatchError(err)
+  );
 }
 
 function isBenignUncaughtNetworkException(err: unknown): boolean {