diff --git a/.changeset/plugin-mode-invalidate.md b/.changeset/plugin-mode-invalidate.md
new file mode 100644
index 000000000..00420bc27
--- /dev/null
+++ b/.changeset/plugin-mode-invalidate.md
@@ -0,0 +1,5 @@
+---
+"webpack-dev-middleware": patch
+---
+
+Fixed a crash when calling `invalidate()` in plugin mode (`isPlugin = true`). Since the host (webpack-cli, webpack-dev-server, etc.) owns `compiler.watch()`, the middleware now invalidates the host's `watching` instead (each child compiler's one for a `MultiCompiler` on webpack < 5.109), and logs a warning when the compiler is not watching at all.
diff --git a/src/index.js b/src/index.js
index c1f485ff4..bcb71108d 100644
--- a/src/index.js
+++ b/src/index.js
@@ -597,9 +597,36 @@ function wdm(compiler, options = {}, isPlugin = false) {
   instance.invalidate = (callback = noop) => {
     middleware.ready(filledContext, callback);
 
-    // TODO for plugin usage (`isPlugin = true`) `watching` is `undefined` and this throws —
-    // invalidate the host's `compiler.watching` (each child's one for a `MultiCompiler`) instead
-    filledContext.watching.invalidate();
+    if (filledContext.watching) {
+      filledContext.watching.invalidate();
+      return;
+    }
+
+    // For plugin usage the host (webpack-cli, webpack-dev-server, etc.) owns
+    // `compiler.watch()`, so invalidate the host's `watching` instead
+    const { compiler: contextCompiler } = filledContext;
+
+    let invalidated = false;
+
+    if (contextCompiler.watching) {
+      contextCompiler.watching.invalidate();
+      invalidated = true;
+    } else if (isMultipleCompiler(contextCompiler)) {
+      // `MultiCompiler` exposes `watching` only since webpack 5.109, fall back
+      // to each child compiler's own `watching`
+      for (const childCompiler of contextCompiler.compilers) {
+        if (childCompiler.watching) {
+          childCompiler.watching.invalidate();
+          invalidated = true;
+        }
+      }
+    }
+
+    if (!invalidated) {
+      filledContext.logger.warn(
+        "The `invalidate` method was called, but the compiler is not watching, so there is nothing to invalidate.",
+      );
+    }
   };
 
   instance.close = (callback = noop) => {
diff --git a/test/__snapshots__/pluginMode.test.js.snap.webpack5 b/test/__snapshots__/pluginMode.test.js.snap.webpack5
index f7a8402c3..360ea9a1a 100644
--- a/test/__snapshots__/pluginMode.test.js.snap.webpack5
+++ b/test/__snapshots__/pluginMode.test.js.snap.webpack5
@@ -3,3 +3,5 @@
 exports[`plugin mode close method should not close the watching owned by the host: warning 1`] = `"The \`close\` method was called, but there is no own \`watching\` instance to close. When using the middleware as a plugin, the host owns watching, so use \`compiler.close()\` instead."`;
 
 exports[`plugin mode close method should not throw and call the callback when the host is not watching: warning 1`] = `"The \`close\` method was called, but there is no own \`watching\` instance to close. When using the middleware as a plugin, the host owns watching, so use \`compiler.close()\` instead."`;
+
+exports[`plugin mode invalidate method should not throw and warn when the host is not watching: warning 1`] = `"The \`invalidate\` method was called, but the compiler is not watching, so there is nothing to invalidate."`;
diff --git a/test/pluginMode.test.js b/test/pluginMode.test.js
index 7600c8758..266cc2b47 100644
--- a/test/pluginMode.test.js
+++ b/test/pluginMode.test.js
@@ -9,6 +9,37 @@ jest.spyOn(globalThis.console, "log").mockImplementation();
 // webpack-dev-server, etc.) owns `compiler.watch()`, so the middleware has no
 // `watching` of its own
 describe("plugin mode", () => {
+  describe("invalidate method", () => {
+    it("should invalidate the watching owned by the host", (done) => {
+      const compiler = getCompiler(webpackConfig);
+      const watching = compiler.watch({}, () => {});
+      const instance = middleware(compiler, {}, true);
+      const invalidateSpy = jest.spyOn(watching, "invalidate");
+
+      instance.waitUntilValid(() => {
+        instance.invalidate();
+
+        expect(invalidateSpy).toHaveBeenCalledTimes(1);
+
+        watching.close(done);
+      });
+    });
+
+    it("should not throw and warn when the host is not watching", () => {
+      const compiler = getCompiler(webpackConfig);
+      const instance = middleware(compiler, {}, true);
+      const warnSpy = jest
+        .spyOn(instance.context.logger, "warn")
+        .mockImplementation();
+
+      expect(() => {
+        instance.invalidate();
+      }).not.toThrow();
+      expect(warnSpy).toHaveBeenCalledTimes(1);
+      expect(warnSpy.mock.calls[0][0]).toMatchSnapshot("warning");
+    });
+  });
+
   describe("close method", () => {
     it("should not throw and call the callback when the host is not watching", (done) => {
       const compiler = getCompiler(webpackConfig);