diff --git a/CHANGELOG.md b/CHANGELOG.md
index 4ba693eb6d5b..90dd8ae840d0 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -22,6 +22,12 @@ Code v99.99.999
 
 ## Unreleased
 
+### Fixed
+
+- `--socket-fd` now works: the inherited socket is passed on to the process
+  that listens, and the address is logged as `fd:<n>`. Previously code-server
+  failed with `listen EEXIST` or `Server has no address`.
+
 ## [4.143.1](https://github.com/coder/code-server/releases/tag/v4.143.1) - 2026-10-23
 
 Code v1.143.1
diff --git a/src/node/app.ts b/src/node/app.ts
index 82b1d2733f13..e995c7c21c0f 100644
--- a/src/node/app.ts
+++ b/src/node/app.ts
@@ -111,9 +111,14 @@ export const createApp = async (args: DefaultedArgs): Promise<App> => {
  *
  * The address might be a URL or it might be a pipe or socket path.
  */
-export const ensureAddress = (server: http.Server, protocol: string): URL | string => {
+export const ensureAddress = (server: http.Server, protocol: string, socketFd?: number): URL | string => {
   const addr = server.address()
 
+  // Node reports no address for a Unix socket adopted by fd.
+  if (!addr && typeof socketFd === "number") {
+    return `fd:${socketFd}`
+  }
+
   if (!addr) {
     throw new Error("Server has no address")
   }
diff --git a/src/node/main.ts b/src/node/main.ts
index c2d3bd57852b..7fcc18b1aad5 100644
--- a/src/node/main.ts
+++ b/src/node/main.ts
@@ -141,7 +141,7 @@ export const runCodeServer = async (
 
   const app = await createApp(args)
   const protocol = args.cert ? "https" : "http"
-  const serverAddress = ensureAddress(app.server, protocol)
+  const serverAddress = ensureAddress(app.server, protocol, args["socket-fd"])
   const { disposeRoutes, heart } = await register(app, args)
 
   logger.info(`Using config file ${args.config}`)
diff --git a/src/node/wrapper.ts b/src/node/wrapper.ts
index 607512e2c9fb..7b0ccb3b9f24 100644
--- a/src/node/wrapper.ts
+++ b/src/node/wrapper.ts
@@ -8,6 +8,9 @@ import { paths } from "./util"
 
 const timeoutInterval = 10000 // 10s, matches VS Code's timeouts.
 
+// Fd 3 in the child is the IPC channel, so the inherited socket goes to fd 4.
+const CHILD_SOCKET_FD = 4
+
 /**
  * Listen to a single message from a process. Reject if the process errors,
  * exits, or times out.
@@ -334,13 +337,14 @@ export class ParentProcess extends Process {
   }
 
   private spawn(): cp.ChildProcess {
+    const socketFd = this.args?.["socket-fd"]
     return cp.fork(path.join(__dirname, "entry"), {
       env: {
         ...process.env,
         CODE_SERVER_PARENT_PID: process.pid.toString(),
         NODE_EXEC_PATH: process.execPath,
       },
-      stdio: ["pipe", "pipe", "pipe", "ipc"],
+      stdio: typeof socketFd === "number" ? ["pipe", "pipe", "pipe", "ipc", socketFd] : ["pipe", "pipe", "pipe", "ipc"],
     })
   }
 
@@ -359,7 +363,8 @@ export class ParentProcess extends Process {
       this.logger,
     )
     this.logger.debug("got message", field("message", message))
-    this.send(child, { type: "handshake", args: this.args })
+    const args = typeof this.args["socket-fd"] === "number" ? { ...this.args, "socket-fd": CHILD_SOCKET_FD } : this.args
+    this.send(child, { type: "handshake", args })
   }
 
   /**
diff --git a/test/integration/socketFd.test.ts b/test/integration/socketFd.test.ts
new file mode 100644
index 000000000000..49edfc691485
--- /dev/null
+++ b/test/integration/socketFd.test.ts
@@ -0,0 +1,80 @@
+import { ChildProcess, spawn } from "child_process"
+import { promises as fs } from "fs"
+import * as http from "http"
+import * as net from "net"
+import * as path from "path"
+import { clean, tmpdir } from "../utils/helpers"
+
+describe("--socket-fd", () => {
+  const testName = "socketFd"
+  const codeServerPath = process.env.CODE_SERVER_PATH || path.resolve("../../release-standalone/bin/code-server")
+  let tempDir: string
+  let socketDir: string | undefined
+  let child: ChildProcess | undefined
+
+  beforeEach(async () => {
+    await clean(testName)
+    tempDir = await tmpdir(testName)
+  })
+
+  afterEach(async () => {
+    if (child?.pid && child.exitCode === null) {
+      // Kill the process group so that the wrapper's inner process also stops.
+      process.kill(-child.pid, "SIGKILL")
+    }
+    if (socketDir) {
+      await fs.rm(socketDir, { force: true, recursive: true })
+      socketDir = undefined
+    }
+  })
+
+  // Give the listener to code-server as fd 3, as systemd socket activation does.
+  const getHealthzThroughFd = async (server: net.Server, target: http.RequestOptions): Promise<number> => {
+    const fd: number = (server as any)._handle.fd
+    let output = ""
+    child = spawn(
+      codeServerPath,
+      [
+        "--socket-fd=3",
+        "--auth=none",
+        `--user-data-dir=${path.join(tempDir, "data")}`,
+        `--config=${path.join(tempDir, "config.yaml")}`,
+      ],
+      { detached: true, stdio: ["ignore", "pipe", "pipe", fd] },
+    )
+    child.stdout?.on("data", (chunk) => (output += chunk))
+    child.stderr?.on("data", (chunk) => (output += chunk))
+    await new Promise((resolve) => server.close(resolve))
+
+    const exited = new Promise<never>((_, reject) => {
+      child?.once("exit", (code) => reject(new Error(`code-server exited with code ${code}:\n${output}`)))
+    })
+    const status = new Promise<number>((resolve, reject) => {
+      http
+        .get({ ...target, path: "/healthz" }, (res) => {
+          res.resume()
+          resolve(res.statusCode ?? 0)
+        })
+        .once("error", (error) => reject(new Error(`${error.message}:\n${output}`)))
+    })
+    return Promise.race([status, exited])
+  }
+
+  it("should serve requests on a Unix socket passed as a file descriptor", async () => {
+    // macOS limits socket paths to 104 bytes, and os.tmpdir() can be too long.
+    socketDir = await fs.mkdtemp("/tmp/cs-fd-")
+    const server = net.createServer()
+    await new Promise<void>((resolve) => server.listen(path.join(socketDir!, "listen.sock"), resolve))
+    // server.close() unlinks the socket path, so connect through a hard link.
+    const socketPath = path.join(socketDir, "connect.sock")
+    await fs.link(path.join(socketDir, "listen.sock"), socketPath)
+    expect(await getHealthzThroughFd(server, { socketPath })).toBe(200)
+  }, 60000)
+
+  it("should serve requests on a TCP socket passed as a file descriptor", async () => {
+    const server = net.createServer()
+    await new Promise<void>((resolve) => server.listen(0, "127.0.0.1", resolve))
+    const { port } = server.address() as net.AddressInfo
+    expect(await getHealthzThroughFd(server, { host: "127.0.0.1", port })).toBe(200)
+  }, 60000)
+})
diff --git a/test/unit/node/app.test.ts b/test/unit/node/app.test.ts
index 54e245aec86c..618771842a4a 100644
--- a/test/unit/node/app.test.ts
+++ b/test/unit/node/app.test.ts
@@ -152,6 +152,9 @@ describe("ensureAddress", () => {
   it("should throw and error if no address", () => {
     expect(() => ensureAddress(mockServer, "http")).toThrow("Server has no address")
   })
+  it("should describe a --socket-fd listener by its fd when node reports no address", () => {
+    expect(ensureAddress(mockServer, "http", 4)).toBe("fd:4")
+  })
   it("should return the address if it's a string", async () => {
     mockServer.address = () => "/path/to/unix.sock"
     const address = ensureAddress(mockServer, "http")