diff --git a/packages/server/src/server/plugins/lifecycle.e2e.test.ts b/packages/server/src/server/plugins/lifecycle.e2e.test.ts
index 05157e3816..aeaa1c79bc 100644
--- a/packages/server/src/server/plugins/lifecycle.e2e.test.ts
+++ b/packages/server/src/server/plugins/lifecycle.e2e.test.ts
@@ -1,6 +1,7 @@
-import { mkdir, mkdtemp, rm, writeFile } from "node:fs/promises";
+import { cp, mkdir, mkdtemp, readFile, rm, writeFile } from "node:fs/promises";
 import { tmpdir } from "node:os";
 import path from "node:path";
+import { fileURLToPath } from "node:url";
 import { expect, onTestFinished, test } from "vitest";
 import { DaemonClient } from "../test-utils/daemon-client.js";
 import { createTestPaseoDaemon } from "../test-utils/paseo-daemon.js";
@@ -457,3 +458,80 @@ test("a provider that never acknowledges session.close does not hold the daemon
   // test fails by timing out.
   await expect(daemon.daemon.stop()).resolves.toBeUndefined();
 }, 90_000);
+
+const repoRoot = fileURLToPath(new URL("../../../../../", import.meta.url));
+
+// Hold the provider close until the subprocess has entered shutdown cleanup.
+async function createSlowClosingProviderPlugin() {
+  const directory = await mkdtemp(path.join(tmpdir(), "paseo-slow-close-plugin-"));
+  const closeStarted = path.join(directory, "close-started");
+  const closeRelease = path.join(directory, "close-release");
+  const cleanupStarted = path.join(directory, "cleanup-started");
+  await cp(path.join(repoRoot, "plugin-examples/provider-direct"), directory, { recursive: true });
+  const providerPath = path.join(directory, "server", "provider.ts");
+  const source = (await readFile(providerPath, "utf8")).replaceAll("\r\n", "\n");
+  const patched = `import { readFile, writeFile } from "node:fs/promises";\n${source.replace(
+    "      closed = true;\n      sessions.clear();",
+    `      closed = true;
+      await writeFile(${JSON.stringify(closeStarted)}, "started");
+      while (true) {
+        try { await readFile(${JSON.stringify(closeRelease)}); break; }
+        catch { await new Promise((resolve) => setTimeout(resolve, 10)); }
+      }
+      sessions.clear();
+      console.log("provider close completed");`,
+  )}`;
+  expect(patched).toContain(`await writeFile(${JSON.stringify(closeStarted)}, "started")`);
+  await writeFile(providerPath, patched);
+  const entryPath = path.join(directory, "index.server.ts");
+  const entry = (await readFile(entryPath, "utf8")).replaceAll("\r\n", "\n");
+  const withCleanup = `import { writeFile } from "node:fs/promises";\n${entry.replace(
+    "  return () => {};",
+    `  return async () => { await writeFile(${JSON.stringify(cleanupStarted)}, "started"); console.log("plugin cleanup completed"); };`,
+  )}`;
+  expect(withCleanup).toContain(`await writeFile(${JSON.stringify(cleanupStarted)}, "started")`);
+  await writeFile(entryPath, withCleanup);
+  return { directory, closeStarted, closeRelease, cleanupStarted };
+}
+
+test("reloading a plugin does not send on a closed IPC channel", async () => {
+  const {
+    directory: pluginDirectory,
+    closeStarted,
+    closeRelease,
+    cleanupStarted,
+  } = await createSlowClosingProviderPlugin();
+  const cwd = await mkdtemp(path.join(tmpdir(), "paseo-reload-teardown-"));
+  const daemon = await createTestPaseoDaemon();
+  const client = new DaemonClient({ url: `ws://127.0.0.1:${daemon.port}/ws` });
+  try {
+    await client.connect();
+    await client.patchDaemonConfig({ pluginsEnabled: true });
+    await client.installDirectoryPlugin(pluginDirectory);
+    const agent = await client.createAgent({ provider: "direct-example", cwd });
+    const turn = client.sendMessage(agent.id, "Say hello").catch(() => undefined);
+    const reload = client.reloadPlugin("provider-direct-example");
+    await expect
+      .poll(() => readFile(closeStarted, "utf8").catch(() => null), { timeout: 20_000 })
+      .toBe("started");
+    await expect
+      .poll(() => readFile(cleanupStarted, "utf8").catch(() => null), { timeout: 20_000 })
+      .toBe("started");
+    await writeFile(closeRelease, "release");
+    const reloaded = await reload;
+    expect(reloaded.status).toBe("running");
+    const entries = await client.getPluginLogs("provider-direct-example");
+    const messages = entries.map((entry) => entry.message).join("\n");
+    expect(messages).not.toContain("ERR_IPC_CHANNEL_CLOSED");
+    expect(entries.filter((entry) => entry.message === "plugin cleanup completed")).toHaveLength(1);
+    expect(entries.filter((entry) => entry.message === "provider close completed")).toHaveLength(1);
+    await turn;
+    await client.archiveAgent(agent.id).catch(() => undefined);
+  } finally {
+    await writeFile(closeRelease, "release");
+    await client.close();
+    await daemon.close();
+    await rm(cwd, { recursive: true, force: true });
+    await rm(pluginDirectory, { recursive: true, force: true });
+  }
+}, 60_000);
diff --git a/packages/server/src/server/plugins/plugin-process.ts b/packages/server/src/server/plugins/plugin-process.ts
index 41310f78e8..1cc0f571a1 100644
--- a/packages/server/src/server/plugins/plugin-process.ts
+++ b/packages/server/src/server/plugins/plugin-process.ts
@@ -51,7 +51,7 @@ const handlers = new Map<string, RegisteredRpc>();
 const providers = new Map<string, ProviderRegistration>();
 const providerConnections = new Map<
   string,
-  { connection: ProviderConnection; unsubscribe: () => void }
+  { connection: ProviderConnection; unsubscribe: () => void; closing?: Promise<void> }
 >();
 const pendingProviderConnections = new Map<string, { tombstoned: boolean }>();
 let cleanup: (() => void | Promise<void>) | null = null;
@@ -193,6 +193,7 @@ async function sendProviderInput(
   if (stopping) throw new Error("Plugin is stopping");
   const current = providerConnections.get(message.connectionId);
   if (!current) throw new Error(`Unknown provider connection: ${message.connectionId}`);
+  if (current.closing) throw new Error("Provider connection is closing");
   await current.connection.send(message.input);
   send({
     type: "provider.accepted",
@@ -201,13 +202,25 @@ async function sendProviderInput(
   });
 }
 
+// The connection stays registered until its close has reported, so shutdown
+// waits for a close already in flight instead of disconnecting underneath it.
 async function closeProviderConnection(connectionId: string): Promise<void> {
   const current = providerConnections.get(connectionId);
   if (!current) return;
-  providerConnections.delete(connectionId);
-  current.unsubscribe();
-  await current.connection.close();
-  send({ type: "provider.closed", connectionId });
+  if (current.closing) return current.closing;
+  const closing = (async () => {
+    current.unsubscribe();
+    try {
+      await current.connection.close();
+      send({ type: "provider.closed", connectionId });
+    } catch (error) {
+      send({ type: "provider.closed", connectionId, error: describeError(error) });
+    } finally {
+      providerConnections.delete(connectionId);
+    }
+  })();
+  current.closing = closing;
+  return closing;
 }
 
 function runtimeRequire(name: string): unknown {
@@ -397,13 +410,7 @@ process.on("message", (rawMessage: unknown) => {
     return;
   }
   if (message.type === "provider.close") {
-    void closeProviderConnection(message.connectionId).catch((error) => {
-      send({
-        type: "provider.closed",
-        connectionId: message.connectionId,
-        error: describeError(error),
-      });
-    });
+    void closeProviderConnection(message.connectionId);
     return;
   }
   if (message.type === "paseo_frame" || message.type === "paseo_close") return;
diff --git a/packages/server/src/server/plugins/runtime.posix.test.ts b/packages/server/src/server/plugins/runtime.posix.test.ts
index 1f82d35909..c09ef9ebe2 100644
--- a/packages/server/src/server/plugins/runtime.posix.test.ts
+++ b/packages/server/src/server/plugins/runtime.posix.test.ts
@@ -34,6 +34,26 @@ async function readTextIfPresent(filePath: string): Promise<string | null> {
   }
 }
 
+function pluginMessages(runtime: PluginRuntime, pluginId: string): string[] {
+  return runtime.getLogs(pluginId).map((entry) => entry.message);
+}
+
+function spawnObservedPluginProcess(onMessage: (message: unknown) => void) {
+  const loaderUrl = new URL("../../terminal/terminal-ts-loader.mjs", import.meta.url).href;
+  const setup = `import { register } from "node:module"; register(${JSON.stringify(loaderUrl)});`;
+  const child = fork(new URL("./plugin-process.ts", import.meta.url), [], {
+    execArgv: [
+      "--experimental-strip-types",
+      "--import",
+      `data:text/javascript,${encodeURIComponent(setup)}`,
+    ],
+    serialization: "advanced",
+    stdio: ["ignore", "pipe", "pipe", "ipc"],
+  });
+  child.on("message", onMessage);
+  return child;
+}
+
 function createReloadChild(
   name: string,
   events: string[],
@@ -1040,6 +1060,75 @@ export default function contribute(plugin: unknown) {
     await rm(cleanupFile, { force: true });
   });
 
+  it("rejects provider input while a connection is closing", async () => {
+    const releaseDirectory = await mkdtemp(path.join(tmpdir(), "paseo-provider-close-"));
+    const releaseFile = path.join(releaseDirectory, "release");
+    const directory = await createPlugin(
+      "closing-provider",
+      `import { readFile, writeFile } from "node:fs/promises";
+import type { ProviderRegistration } from "@getpaseo/plugin/server/provider";
+const provider: ProviderRegistration = {
+  id: "delayed",
+  label: "Delayed",
+  async connect() {
+    return {
+      version: 1,
+      capabilities: [],
+      async send() { console.log("provider accepted input"); },
+      onEvent() { return () => undefined; },
+      async close() {
+        console.log("provider close started");
+        while (true) {
+          try { await readFile(${JSON.stringify(releaseFile)}); break; }
+          catch { await new Promise((resolve) => setTimeout(resolve, 10)); }
+        }
+        console.log("provider close completed");
+      },
+    };
+  },
+};
+export default function contribute(server: { registerProvider(provider: ProviderRegistration): void }) {
+  server.registerProvider(provider);
+  return () => console.log("plugin cleanup started");
+}`,
+    );
+    const closedReports: unknown[] = [];
+    const observeMessage = (message: unknown) => {
+      if ((message as { type?: string }).type === "provider.closed") closedReports.push(message);
+    };
+    const runtime = createTestRuntime({
+      spawnChild: () => spawnObservedPluginProcess(observeMessage),
+    });
+    await runtime.startPlugin("closing-provider", directory);
+    try {
+      const connection = await runtime.connectProvider("closing-provider", "delayed", {
+        versions: [1],
+        capabilities: [],
+      });
+      const closing = connection.close();
+      await expect
+        .poll(() => pluginMessages(runtime, "closing-provider"))
+        .toContain("provider close started");
+      await expect(connection.send({ type: "catalog", requestId: "during-close" })).rejects.toThrow(
+        "Provider connection is closing",
+      );
+      const stopping = runtime.stopPluginById("closing-provider");
+      await expect
+        .poll(() => pluginMessages(runtime, "closing-provider"))
+        .toContain("plugin cleanup started");
+      await writeFile(releaseFile, "release");
+      await Promise.all([closing, stopping]);
+      const messages = pluginMessages(runtime, "closing-provider");
+      expect(messages).toContain("provider close completed");
+      expect(messages).not.toContain("provider accepted input");
+      expect(closedReports).toHaveLength(1);
+    } finally {
+      await writeFile(releaseFile, "release");
+      await runtime.stopAll();
+      await rm(releaseDirectory, { recursive: true, force: true });
+    }
+  });
+
   it("closes a provider connection that resolves during plugin shutdown", async () => {
     const suffix = `${process.pid}-${Date.now()}`;
     const startedFile = path.join(tmpdir(), `paseo-provider-connect-started-${suffix}`);