diff --git a/packages/webpack-cli/src/webpack-cli.ts b/packages/webpack-cli/src/webpack-cli.ts
index dd88847a165..e1b64f3277c 100644
--- a/packages/webpack-cli/src/webpack-cli.ts
+++ b/packages/webpack-cli/src/webpack-cli.ts
@@ -1678,6 +1678,7 @@ class WebpackCLI {
         const compilersForDevServer =
           possibleCompilers.length > 0 ? possibleCompilers : [compilers[0]];
         const usedPorts: number[] = [];
+        const usedPublicPathsByPort = new Map<number, Set<string> | null>();
 
         for (const compilerForDevServer of compilersForDevServer) {
           if (compilerForDevServer.options.devServer === false) {
@@ -1710,11 +1711,37 @@ class WebpackCLI {
 
           if (devServerConfiguration.port) {
             const portNumber = Number(devServerConfiguration.port);
+            const devMiddlewarePublicPath = devServerConfiguration.devMiddleware?.publicPath;
+            const outputPublicPath = compilerForDevServer.options.output?.publicPath;
+            const currentPublicPath =
+              typeof devMiddlewarePublicPath === "string"
+                ? devMiddlewarePublicPath
+                : typeof outputPublicPath === "string"
+                  ? outputPublicPath
+                  : undefined;
 
             if (usedPorts.includes(portNumber)) {
-              throw new Error(
-                "Unique ports must be specified for each devServer option in your webpack configuration. Alternatively, run only 1 devServer config using the --config-name flag to specify your desired config.",
-              );
+              const usedPublicPaths = usedPublicPathsByPort.get(portNumber);
+
+              if (
+                !currentPublicPath ||
+                !usedPublicPaths ||
+                usedPublicPaths.has(currentPublicPath)
+              ) {
+                throw new Error(
+                  "Unique ports must be specified for each devServer option in your webpack configuration. Alternatively, use unique devMiddleware.publicPath/output.publicPath values for configs sharing a port, or run only 1 devServer config using the --config-name flag to specify your desired config.",
+                );
+              }
+
+              usedPublicPaths.add(currentPublicPath);
+
+              continue;
+            }
+
+            if (currentPublicPath) {
+              usedPublicPathsByPort.set(portNumber, new Set([currentPublicPath]));
+            } else {
+              usedPublicPathsByPort.set(portNumber, null);
             }
 
             usedPorts.push(portNumber);
diff --git a/test/serve/basic/__snapshots__/serve-basic.test.js.snap.devServer5.webpack5 b/test/serve/basic/__snapshots__/serve-basic.test.js.snap.devServer5.webpack5
index 4f18e0f6b3e..c7853395b42 100644
--- a/test/serve/basic/__snapshots__/serve-basic.test.js.snap.devServer5.webpack5
+++ b/test/serve/basic/__snapshots__/serve-basic.test.js.snap.devServer5.webpack5
@@ -71,7 +71,7 @@ exports[`basic serve usage should throw error when same ports in multicompiler:
 <i> [webpack-dev-server] On Your Network (IPv4): http://x.x.x.x:<port>/
 <i> [webpack-dev-server] On Your Network (IPv6): http://[x:x:x:x:x:x:x:x]:<port>/
 <i> [webpack-dev-server] Content not from webpack is served from '<cwd>/test/serve/basic/public' directory
-[webpack-cli] Error: Unique ports must be specified for each devServer option in your webpack configuration. Alternatively, run only 1 devServer config using the --config-name flag to specify your desired config.
+[webpack-cli] Error: Unique ports must be specified for each devServer option in your webpack configuration. Alternatively, use unique devMiddleware.publicPath/output.publicPath values for configs sharing a port, or run only 1 devServer config using the --config-name flag to specify your desired config.
     at stack"
 `;
 
@@ -92,6 +92,14 @@ exports[`basic serve usage should work in multi compiler mode: stderr 1`] = `
 <i> [webpack-dev-server] Content not from webpack is served from '<cwd>/test/serve/basic/public' directory"
 `;
 
+exports[`basic serve usage should work when same ports in multicompiler with unique public paths: stderr 1`] = `
+"<i> [webpack-dev-server] Project is running at:
+<i> [webpack-dev-server] Loopback: http://localhost:<port>/, http://[::1]:<port>/
+<i> [webpack-dev-server] On Your Network (IPv4): http://x.x.x.x:<port>/
+<i> [webpack-dev-server] On Your Network (IPv6): http://[x:x:x:x:x:x:x:x]:<port>/
+<i> [webpack-dev-server] Content not from webpack is served from '<cwd>/test/serve/basic/public' directory"
+`;
+
 exports[`basic serve usage should work with "--hot" and "--port" options: stderr 1`] = `
 "<i> [webpack-dev-server] Project is running at:
 <i> [webpack-dev-server] Loopback: http://localhost:<port>/, http://[::1]:<port>/
diff --git a/test/serve/basic/same-ports-dev-server-unique-public-paths.config.js b/test/serve/basic/same-ports-dev-server-unique-public-paths.config.js
new file mode 100644
index 00000000000..e44ae51eeb9
--- /dev/null
+++ b/test/serve/basic/same-ports-dev-server-unique-public-paths.config.js
@@ -0,0 +1,48 @@
+const WebpackCLITestPlugin = require("../../utils/webpack-cli-test-plugin");
+const devServerConfig = require("./helper/base-dev-server.config");
+
+const getGetPort = () => import("get-port");
+
+module.exports = async () => {
+  const sharedPort = await (await getGetPort()).default();
+
+  return [
+    {
+      name: "one",
+      mode: "development",
+      devtool: false,
+      output: {
+        publicPath: "/login/",
+        filename: "first-output/[name].js",
+      },
+      devServer: {
+        ...devServerConfig,
+        port: sharedPort,
+        devMiddleware: {
+          ...devServerConfig.devMiddleware,
+          publicPath: "/login/",
+        },
+      },
+      plugins: [new WebpackCLITestPlugin(["mode", "output"], false, "hooks.compilation.taps")],
+    },
+    {
+      name: "two",
+      mode: "development",
+      devtool: false,
+      entry: "./src/other.js",
+      output: {
+        publicPath: "/admin/",
+        filename: "second-output/[name].js",
+      },
+      devServer: {
+        ...devServerConfig,
+        port: sharedPort,
+        devMiddleware: {
+          ...devServerConfig.devMiddleware,
+          publicPath: "/admin/",
+        },
+      },
+      plugins: [new WebpackCLITestPlugin(["mode", "output"], false, "hooks.compilation.taps")],
+    },
+  ];
+};
diff --git a/test/serve/basic/serve-basic.test.js b/test/serve/basic/serve-basic.test.js
index 3a40429160a..4512850b287 100644
--- a/test/serve/basic/serve-basic.test.js
+++ b/test/serve/basic/serve-basic.test.js
@@ -506,4 +506,16 @@ describe("basic serve usage", () => {
     // Due to racing logic, first dev server can be started and compiled, but then the second always fails
     // expect(normalizeStdout(stdout)).toMatchSnapshot("stdout");
   });
+
+  it("should work when same ports in multicompiler with unique public paths", async () => {
+    const { stderr, stdout } = await runWatch(
+      __dirname,
+      ["serve", "--config", "same-ports-dev-server-unique-public-paths.config.js"],
+      normalStdKillOptions,
+    );
+
+    expect(normalizeStderr(stderr)).toMatchSnapshot("stderr");
+    expect(stderr).not.toContain("Unique ports must be specified");
+    expect(stdout).toBeDefined();
+  });
 });