diff --git a/.cspell.json b/.cspell.json
index c4133a96b2..730420f579 100644
--- a/.cspell.json
+++ b/.cspell.json
@@ -19,6 +19,7 @@
     "colorette",
     "selfsigned",
     "portfinder",
+    "watchings",
     "xlink",
     "instanceof",
     "Heyo",
diff --git a/lib/Server.js b/lib/Server.js
index db89afbb02..38577856c9 100644
--- a/lib/Server.js
+++ b/lib/Server.js
@@ -3466,6 +3466,45 @@ class Server {
    * @param {import("webpack-dev-middleware").Callback=} callback callback
    */
   invalidate(callback = () => {}) {
+    // In plugin mode the host owns `compiler.watch()`, so the middleware has no
+    // `watching` of its own — invalidate the host's watching(s) directly to
+    // trigger a rebuild (each child's own `watching` for a `MultiCompiler`).
+    if (this.isPlugin) {
+      const compilers =
+        /** @type {MultiCompiler} */ (this.compiler).compilers ||
+        /** @type {Compiler[]} */ ([this.compiler]);
+
+      /** @type {NonNullable<Compiler["watching"]>[]} */
+      const watchings = [];
+
+      for (const compiler of compilers) {
+        if (compiler.watching) {
+          watchings.push(compiler.watching);
+        }
+      }
+
+      if (watchings.length === 0) {
+        callback();
+        return;
+      }
+
+      let pending = watchings.length;
+
+      const onInvalidated = () => {
+        pending -= 1;
+
+        if (pending === 0) {
+          callback();
+        }
+      };
+
+      for (const watching of watchings) {
+        watching.invalidate(onInvalidated);
+      }
+
+      return;
+    }
+
     if (this.middleware) {
       this.middleware.invalidate(callback);
     }
@@ -3660,19 +3699,23 @@ class Server {
       );
 
       if (this.middleware) {
-        await /** @type {Promise<void>} */ (
-          new Promise((resolve, reject) => {
-            /** @type {import("webpack-dev-middleware").API<Request, Response>} */
-            (this.middleware).close((error) => {
-              if (error) {
-                reject(error);
-                return;
-              }
+        // In plugin mode the middleware has no `watching` of its own to close
+        // (the host's `compiler.close()` handles it).
+        if (!this.isPlugin) {
+          await /** @type {Promise<void>} */ (
+            new Promise((resolve, reject) => {
+              /** @type {import("webpack-dev-middleware").API<Request, Response>} */
+              (this.middleware).close((error) => {
+                if (error) {
+                  reject(error);
+                  return;
+                }
 
-              resolve();
-            });
-          })
-        );
+                resolve();
+              });
+            })
+          );
+        }
 
         this.middleware = undefined;
       }
diff --git a/test/e2e/api-plugin.test.js b/test/e2e/api-plugin.test.js
index 1d786ca818..405f828429 100644
--- a/test/e2e/api-plugin.test.js
+++ b/test/e2e/api-plugin.test.js
@@ -1,4 +1,5 @@
 import fs from "node:fs";
+import http from "node:http";
 import os from "node:os";
 import path from "node:path";
 import { afterEach, beforeEach, describe, it } from "node:test";
@@ -109,6 +110,23 @@ describe("API (plugin)", () => {
     stopSpy.mockRestore();
   });
 
+  it("should tear down without error when the compiler is closed", async () => {
+    // In plugin mode the host owns `watching`, so `stop()` must not call
+    // `middleware.close()` — otherwise `compiler.close` surfaces a TypeError.
+    const compiler = webpack(config);
+    const server = new Server({ port });
+
+    server.apply(compiler);
+
+    await compile(compiler, port);
+
+    const closeError = await new Promise((resolve) => {
+      compiler.close((error) => resolve(error));
+    });
+
+    expect(closeError).toBeFalsy();
+  });
+
   it("should stay passive in build mode (compiler.run)", async () => {
     // The shared fixture writes output to "/", which would be unwritable
     // outside of webpack-dev-middleware's in-memory FS. Use a tmp dir so the
@@ -227,6 +245,134 @@ describe("API (plugin)", () => {
     });
   });
 
+  it("should trigger a rebuild via `server.invalidate()` in plugin mode", async () => {
+    const compiler = webpack(config);
+    const server = new Server({ port });
+    server.apply(compiler);
+
+    await compile(compiler, port);
+
+    const sawInvalid = await new Promise((resolve, reject) => {
+      let initialOkSeen = false;
+      const ws = new WebSocket(`ws://127.0.0.1:${port}/ws`, {
+        headers: {
+          host: `127.0.0.1:${port}`,
+          origin: `http://127.0.0.1:${port}`,
+        },
+      });
+
+      ws.on("error", reject);
+      ws.on("message", (raw) => {
+        const { type } = JSON.parse(raw.toString());
+
+        if (!initialOkSeen && type === "ok") {
+          initialOkSeen = true;
+          // Must invalidate the host's `watching` (the middleware has none in
+          // plugin mode) instead of throwing.
+          server.invalidate();
+          return;
+        }
+
+        if (type === "invalid") {
+          ws.close();
+          resolve(true);
+        }
+      });
+    });
+
+    expect(sawInvalid).toBe(true);
+
+    await new Promise((resolve) => {
+      compiler.close(resolve);
+    });
+  });
+
+  it("should trigger a rebuild via the /webpack-dev-server/invalidate route in plugin mode", async () => {
+    const compiler = webpack(config);
+    const server = new Server({ port });
+    server.apply(compiler);
+
+    await compile(compiler, port);
+
+    const sawInvalid = await new Promise((resolve, reject) => {
+      let initialOkSeen = false;
+      const ws = new WebSocket(`ws://127.0.0.1:${port}/ws`, {
+        headers: {
+          host: `127.0.0.1:${port}`,
+          origin: `http://127.0.0.1:${port}`,
+        },
+      });
+
+      ws.on("error", reject);
+      ws.on("message", (raw) => {
+        const { type } = JSON.parse(raw.toString());
+
+        if (!initialOkSeen && type === "ok") {
+          initialOkSeen = true;
+          // Hit the route as a browser would (same-origin, so it passes the
+          // cross-origin check) — it must trigger a rebuild, not crash.
+          http
+            .get(
+              `http://127.0.0.1:${port}/webpack-dev-server/invalidate`,
+              {
+                headers: {
+                  host: `127.0.0.1:${port}`,
+                  origin: `http://127.0.0.1:${port}`,
+                },
+              },
+              (res) => res.resume(),
+            )
+            .on("error", reject);
+          return;
+        }
+
+        if (type === "invalid") {
+          ws.close();
+          resolve(true);
+        }
+      });
+    });
+
+    expect(sawInvalid).toBe(true);
+
+    await new Promise((resolve) => {
+      compiler.close(resolve);
+    });
+  });
+
+  it("should invoke the callback after `server.invalidate()` rebuilds in plugin mode", async () => {
+    const compiler = webpack(config);
+    const server = new Server({ port });
+    server.apply(compiler);
+
+    await compile(compiler, port);
+
+    // The callback fires once the invalidated build finishes.
+    await new Promise((resolve) => {
+      server.invalidate(resolve);
+    });
+
+    await new Promise((resolve) => {
+      compiler.close(resolve);
+    });
+  });
+
+  it("should invoke the callback when `server.invalidate()` runs with no active watching", async () => {
+    const compiler = webpack(config);
+    const server = new Server({ port });
+    server.apply(compiler);
+
+    // No `compiler.watch()` — there is no `watching`, so invalidate is a no-op
+    // that still calls the callback.
+    await new Promise((resolve) => {
+      server.invalidate(resolve);
+    });
+
+    await new Promise((resolve) => {
+      compiler.close(resolve);
+    });
+  });
+
   it("should use constructor options instead of compiler.options.devServer", async () => {
     // Plugin reads its options from its constructor argument; values on
     // `compiler.options.devServer` are intentionally ignored. This protects