diff --git a/server/src/__tests__/plugin-dev-watcher.test.ts b/server/src/__tests__/plugin-dev-watcher.test.ts
index 75df3105535..c6ffa74257d 100644
--- a/server/src/__tests__/plugin-dev-watcher.test.ts
+++ b/server/src/__tests__/plugin-dev-watcher.test.ts
@@ -1,12 +1,28 @@
 import { mkdtempSync, mkdirSync, rmSync, writeFileSync } from "node:fs";
+import { EventEmitter } from "node:events";
 import os from "node:os";
 import path from "node:path";
-import { afterEach, describe, expect, it } from "vitest";
-import { resolvePluginWatchTargets } from "../services/plugin-dev-watcher.js";
+import { afterEach, beforeEach, describe, expect, it, vi } from "vitest";
+
+const chokidarMock = vi.hoisted(() => ({
+  watch: vi.fn(),
+}));
+
+vi.mock("chokidar", () => ({
+  default: chokidarMock,
+}));
+
+import { createPluginDevWatcher, resolvePluginWatchTargets } from "../services/plugin-dev-watcher.js";
 
 const tempDirs: string[] = [];
 
+beforeEach(() => {
+  vi.useRealTimers();
+  chokidarMock.watch.mockReset();
+});
+
 afterEach(() => {
+  vi.useRealTimers();
   while (tempDirs.length > 0) {
     const dir = tempDirs.pop();
     if (dir) rmSync(dir, { recursive: true, force: true });
@@ -19,25 +35,49 @@ function makeTempPluginDir(): string {
   return dir;
 }
 
+function writePluginPackage(pluginDir: string): void {
+  mkdirSync(path.join(pluginDir, "dist", "ui"), { recursive: true });
+  writeFileSync(
+    path.join(pluginDir, "package.json"),
+    JSON.stringify({
+      name: "@acme/example",
+      paperclipPlugin: {
+        manifest: "./dist/manifest.js",
+        worker: "./dist/worker.js",
+        ui: "./dist/ui",
+      },
+    }),
+  );
+  writeFileSync(path.join(pluginDir, "dist", "manifest.js"), "export default {};\n");
+  writeFileSync(path.join(pluginDir, "dist", "worker.js"), "export default {};\n");
+  writeFileSync(path.join(pluginDir, "dist", "ui", "index.js"), "export default {};\n");
+  writeFileSync(path.join(pluginDir, "dist", "ui", "index.css"), "body {}\n");
+}
+
+function createLifecycle() {
+  const emitter = new EventEmitter();
+  return Object.assign(emitter, {
+    restartWorker: vi.fn().mockResolvedValue(undefined),
+  });
+}
+
+function installMockFsWatcher() {
+  const handlers: Record<string, (...args: unknown[]) => void> = {};
+  const fakeWatcher = {
+    close: vi.fn(),
+    on: vi.fn((event: string, listener: (...args: unknown[]) => void) => {
+      handlers[event] = listener;
+      return fakeWatcher;
+    }),
+  };
+  chokidarMock.watch.mockReturnValue(fakeWatcher);
+  return { fakeWatcher, handlers };
+}
+
 describe("resolvePluginWatchTargets", () => {
   it("watches package metadata plus concrete declared runtime files", () => {
     const pluginDir = makeTempPluginDir();
-    mkdirSync(path.join(pluginDir, "dist", "ui"), { recursive: true });
-    writeFileSync(
-      path.join(pluginDir, "package.json"),
-      JSON.stringify({
-        name: "@acme/example",
-        paperclipPlugin: {
-          manifest: "./dist/manifest.js",
-          worker: "./dist/worker.js",
-          ui: "./dist/ui",
-        },
-      }),
-    );
-    writeFileSync(path.join(pluginDir, "dist", "manifest.js"), "export default {};\n");
-    writeFileSync(path.join(pluginDir, "dist", "worker.js"), "export default {};\n");
-    writeFileSync(path.join(pluginDir, "dist", "ui", "index.js"), "export default {};\n");
-    writeFileSync(path.join(pluginDir, "dist", "ui", "index.css"), "body {}\n");
+    writePluginPackage(pluginDir);
 
     const targets = resolvePluginWatchTargets(pluginDir);
 
@@ -66,3 +106,43 @@ describe("resolvePluginWatchTargets", () => {
     ]);
   });
 });
+
+describe("createPluginDevWatcher", () => {
+  it("starts watching local plugins announced by lifecycle events", async () => {
+    const pluginDir = makeTempPluginDir();
+    writePluginPackage(pluginDir);
+    installMockFsWatcher();
+    const lifecycle = createLifecycle();
+
+    const devWatcher = createPluginDevWatcher(
+      lifecycle as never,
+      async (pluginId) => (pluginId === "plugin-1" ? pluginDir : null),
+    );
+
+    lifecycle.emit("plugin.loaded", { pluginId: "plugin-1", pluginKey: "example" });
+
+    await vi.waitFor(() => expect(chokidarMock.watch).toHaveBeenCalledTimes(1));
+    const [watchedPaths] = chokidarMock.watch.mock.calls[0] ?? [];
+    expect(watchedPaths).toContain(path.join(pluginDir, "dist", "worker.js"));
+
+    devWatcher.close();
+  });
+
+  it("debounces watched file changes and restarts the plugin worker", async () => {
+    vi.useFakeTimers();
+    const pluginDir = makeTempPluginDir();
+    writePluginPackage(pluginDir);
+    const { handlers } = installMockFsWatcher();
+    const lifecycle = createLifecycle();
+
+    const devWatcher = createPluginDevWatcher(lifecycle as never);
+    devWatcher.watch("plugin-1", pluginDir);
+
+    handlers.all?.("change", path.join(pluginDir, "dist", "worker.js"));
+    await vi.advanceTimersByTimeAsync(500);
+
+    expect(lifecycle.restartWorker).toHaveBeenCalledWith("plugin-1");
+
+    devWatcher.close();
+  });
+});
diff --git a/server/src/app.ts b/server/src/app.ts
index d94475afeab..d037718420f 100644
--- a/server/src/app.ts
+++ b/server/src/app.ts
@@ -420,12 +420,10 @@ export async function createApp(
   void toolDispatcher.initialize().catch((err) => {
     logger.error({ err }, "Failed to initialize plugin tool dispatcher");
   });
-  const devWatcher = opts.uiMode === "vite-dev"
-    ? createPluginDevWatcher(
-      lifecycle,
-      async (pluginId) => (await pluginRegistry.getById(pluginId))?.packagePath ?? null,
-    )
-    : null;
+  const devWatcher = createPluginDevWatcher(
+    lifecycle,
+    async (pluginId) => (await pluginRegistry.getById(pluginId))?.packagePath ?? null,
+  );
   void loader.loadAll().then((result) => {
     if (!result) return;
     for (const loaded of result.results) {
diff --git a/server/src/services/plugin-dev-watcher.ts b/server/src/services/plugin-dev-watcher.ts
index 76b258c4218..ceba5d4e181 100644
--- a/server/src/services/plugin-dev-watcher.ts
+++ b/server/src/services/plugin-dev-watcher.ts
@@ -164,6 +164,10 @@ export function createPluginDevWatcher(
   const watchers = new Map<string, FSWatcher>();
   const debounceTimers = new Map<string, ReturnType<typeof setTimeout>>();
   const fileExists = fsDeps?.existsSync ?? existsSync;
+  log.info(
+    { resolvesInstalledPlugins: Boolean(resolvePluginPackagePath) },
+    "plugin-dev-watcher: initialized",
+  );
 
   function watchPlugin(pluginId: string, packagePath: string): void {
     // Don't double-watch
@@ -293,11 +297,23 @@ export function createPluginDevWatcher(
   }
 
   async function watchLocalPluginById(pluginId: string): Promise<void> {
-    if (!resolvePluginPackagePath) return;
+    if (!resolvePluginPackagePath) {
+      log.debug(
+        { pluginId },
+        "plugin-dev-watcher: no package path resolver configured, skipping lifecycle event",
+      );
+      return;
+    }
 
     try {
       const packagePath = await resolvePluginPackagePath(pluginId);
-      if (!packagePath) return;
+      if (!packagePath) {
+        log.debug(
+          { pluginId },
+          "plugin-dev-watcher: plugin is not a local-path install, skipping watch",
+        );
+        return;
+      }
       watchPlugin(pluginId, packagePath);
     } catch (err) {
       log.warn(