diff --git a/server/src/__tests__/plugin-lifecycle-restart.test.ts b/server/src/__tests__/plugin-lifecycle-restart.test.ts
new file mode 100644
index 00000000000..d7731fde1fa
--- /dev/null
+++ b/server/src/__tests__/plugin-lifecycle-restart.test.ts
@@ -0,0 +1,115 @@
+/**
+ * Regression test for PAP-9585.
+ *
+ * `restartWorker` is called by the dev file-watcher whenever a local-path
+ * plugin's source files change. Before PAP-9585 it only bounced the worker
+ * subprocess, which left newly added `migrations/*.sql` files unapplied — the
+ * plugin schema would silently drift out of sync with worker code.
+ *
+ * The fix is for `restartWorker` to do a full deactivate + reactivate cycle
+ * via the plugin loader, which re-reads the manifest from disk and runs
+ * `applyMigrations` (idempotently) before starting the new worker.
+ */
+import { describe, expect, it, vi } from "vitest";
+
+const pluginRecord = {
+  id: "plugin-1",
+  pluginKey: "example.plugin",
+  status: "ready",
+  manifestJson: { id: "example.plugin", capabilities: [] },
+  packageName: "@example/plugin",
+  version: "1.0.0",
+  packagePath: "/tmp/example-plugin",
+};
+
+const mockRegistry = vi.hoisted(() => ({
+  getById: vi.fn(),
+  getByKey: vi.fn(),
+  update: vi.fn(),
+  updateStatus: vi.fn(),
+  upsertConfig: vi.fn(),
+  getConfig: vi.fn(),
+  list: vi.fn(),
+  delete: vi.fn(),
+}));
+
+vi.mock("../services/plugin-registry.js", () => ({
+  pluginRegistryService: () => mockRegistry,
+}));
+
+import { pluginLifecycleManager } from "../services/plugin-lifecycle.js";
+import type { PluginLoader } from "../services/plugin-loader.js";
+import type { PluginWorkerManager } from "../services/plugin-worker-manager.js";
+
+function makeWorkerManagerStub() {
+  const handle = {
+    restart: vi.fn().mockResolvedValue(undefined),
+    stop: vi.fn().mockResolvedValue(undefined),
+  };
+  return {
+    handle,
+    workerManager: {
+      getWorker: vi.fn().mockReturnValue(handle),
+      isRunning: vi.fn().mockReturnValue(true),
+      startWorker: vi.fn().mockResolvedValue(undefined),
+      stopWorker: vi.fn().mockResolvedValue(undefined),
+      restartWorker: vi.fn().mockResolvedValue(undefined),
+    } as unknown as PluginWorkerManager,
+  };
+}
+
+describe("pluginLifecycleManager.restartWorker", () => {
+  it("does a full deactivate+reactivate cycle when the loader has runtime services", async () => {
+    mockRegistry.getById.mockResolvedValue(pluginRecord);
+    mockRegistry.updateStatus.mockResolvedValue(pluginRecord);
+
+    const { handle, workerManager } = makeWorkerManagerStub();
+
+    const loader: Partial<PluginLoader> = {
+      hasRuntimeServices: vi.fn().mockReturnValue(true) as PluginLoader["hasRuntimeServices"],
+      loadSingle: vi.fn().mockResolvedValue({
+        success: true,
+        plugin: pluginRecord,
+        registered: { worker: true, eventSubscriptions: 0, jobs: 0, webhooks: 0, tools: 0 },
+      }) as PluginLoader["loadSingle"],
+      unloadSingle: vi.fn().mockResolvedValue(undefined) as PluginLoader["unloadSingle"],
+    };
+
+    const lifecycle = pluginLifecycleManager(
+      {} as never,
+      { loader: loader as PluginLoader, workerManager },
+    );
+
+    await lifecycle.restartWorker("plugin-1");
+
+    expect(loader.unloadSingle).toHaveBeenCalledWith("plugin-1", "example.plugin");
+    expect(loader.loadSingle).toHaveBeenCalledWith("plugin-1");
+    // The bare worker handle should NOT be bounced — the loader handles
+    // worker (re)start as part of activate.
+    expect(handle.restart).not.toHaveBeenCalled();
+  });
+
+  it("falls back to bouncing the worker handle when the loader has no runtime services", async () => {
+    mockRegistry.getById.mockResolvedValue(pluginRecord);
+    mockRegistry.updateStatus.mockResolvedValue(pluginRecord);
+
+    const { handle, workerManager } = makeWorkerManagerStub();
+
+    const loader: Partial<PluginLoader> = {
+      hasRuntimeServices: vi.fn().mockReturnValue(false) as PluginLoader["hasRuntimeServices"],
+      loadSingle: vi.fn() as PluginLoader["loadSingle"],
+      unloadSingle: vi.fn() as PluginLoader["unloadSingle"],
+    };
+
+    const lifecycle = pluginLifecycleManager(
+      {} as never,
+      { loader: loader as PluginLoader, workerManager },
+    );
+
+    await lifecycle.restartWorker("plugin-1");
+
+    expect(loader.unloadSingle).not.toHaveBeenCalled();
+    expect(loader.loadSingle).not.toHaveBeenCalled();
+    expect(handle.restart).toHaveBeenCalledTimes(1);
+  });
+});
diff --git a/server/src/services/plugin-lifecycle.ts b/server/src/services/plugin-lifecycle.ts
index e9f9b02b125..daee94173c2 100644
--- a/server/src/services/plugin-lifecycle.ts
+++ b/server/src/services/plugin-lifecycle.ts
@@ -776,19 +776,48 @@ export function pluginLifecycleManager(
         );
       }
 
-      log.info(
-        { pluginId, pluginKey: plugin.pluginKey },
-        "plugin lifecycle: restarting worker",
-      );
+      const supportsRuntimeActivation =
+        typeof pluginLoaderInstance.hasRuntimeServices === "function"
+        && typeof pluginLoaderInstance.loadSingle === "function"
+        && typeof pluginLoaderInstance.unloadSingle === "function"
+        && pluginLoaderInstance.hasRuntimeServices();
 
-      await handle.restart();
+      if (supportsRuntimeActivation) {
+        log.info(
+          { pluginId, pluginKey: plugin.pluginKey },
+          "plugin lifecycle: reloading plugin (re-reading manifest, re-applying pending migrations, restarting worker)",
+        );
+
+        // Full deactivate+reactivate cycle (not just `handle.restart()`) so that:
+        //   - the manifest is re-read from disk, picking up newly declared
+        //     `migrations/*.sql` files and any other manifest changes,
+        //   - `applyMigrations` runs idempotently against the up-to-date
+        //     migrations directory — pending migrations get applied, already-
+        //     applied ones are skipped via the `pluginMigrations` table,
+        //   - the worker subprocess is replaced with one loading the freshly
+        //     built bundle.
+        //
+        // Bouncing the worker process alone (`handle.restart()`) leaves plugin
+        // schema out of sync with worker code whenever a hot reload adds a new
+        // migration, which makes downstream queries fail against missing tables.
+        await deactivatePluginRuntime(pluginId, plugin.pluginKey);
+        await activateReadyPlugin(pluginId);
+      } else {
+        // No runtime activation services wired in (e.g. state-only test harness)
+        // — fall back to a bare worker subprocess bounce.
+        log.info(
+          { pluginId, pluginKey: plugin.pluginKey },
+          "plugin lifecycle: restarting worker (runtime services unavailable; skipping migration re-apply)",
+        );
+        await handle.restart();
+      }
 
       emitDomain("plugin.worker_stopped", { pluginId, pluginKey: plugin.pluginKey });
       emitDomain("plugin.worker_started", { pluginId, pluginKey: plugin.pluginKey });
 
       log.info(
         { pluginId, pluginKey: plugin.pluginKey },
-        "plugin lifecycle: worker restarted",
+        "plugin lifecycle: plugin reloaded",
       );
     },