diff --git a/go/handoff/handoff.go b/go/handoff/handoff.go
new file mode 100644
index 00000000000..455e9440134
--- /dev/null
+++ b/go/handoff/handoff.go
@@ -0,0 +1,179 @@
+package handoff
+
+import (
+	"errors"
+	"fmt"
+	"net"
+	"os"
+	"syscall"
+	"time"
+
+	"golang.org/x/sys/unix"
+
+	"vitess.io/vitess/go/vt/log"
+)
+
+// handoff implements a no-downtime handoff of a TCP listener from one running
+// process to another. It can be used for no-downtime deploys of HTTP servers
+// on a single host/port.
+
+// Listen opens a unix domain socket and listens for handoff requests. When a
+// handoff request is received, the underlying file descriptor of `listener` is
+// handed off over the socket.
+//
+// If an error occurs while opening the unix domain
+// socket, or during handoff, it will be logged and the listener will resume
+// listening. Otherwise, Listen will return nil when the handoff is complete.
+//
+// Callers should drain any servers
+// connected to the net.Listener, and in-flight requests should be resolved
+// before shutting down.
+func Listen(socketPath string, listener net.Listener) error {
+	// Clean up any leftover sockets that might have gotten left from previous
+	// processes.
+	os.Remove(socketPath)
+
+	unixListener, err := net.Listen("unix", socketPath)
+	if err != nil {
+		return err
+	}
+	defer func() {
+		unixListener.Close()
+		os.Remove(socketPath)
+	}()
+
+	for {
+		err := listen(unixListener, listener)
+		if err != nil {
+			log.Error("handoff socket error", "error", err)
+			continue
+		}
+
+		return nil
+	}
+}
+
+var magicPacket = "handoff"
+
+func listen(unixListener, listener net.Listener) error {
+	conn, err := unixListener.Accept()
+	if err != nil {
+		return err
+	}
+	defer conn.Close()
+	err = conn.SetDeadline(time.Now().Add(1 * time.Second))
+	if err != nil {
+		return err
+	}
+
+	b := make([]byte, len(magicPacket))
+	n, err := conn.Read(b)
+	if err != nil {
+		return err
+	}
+	if string(b[:n]) != magicPacket {
+		return errors.New("bad magic packet")
+	}
+
+	return handoff(conn, listener)
+}
+
+func handoff(conn net.Conn, listener net.Listener) error {
+	unixFD, err := getFD(conn.(*net.UnixConn))
+	if err != nil {
+		return err
+	}
+
+	tcpListener := listener.(*net.TCPListener)
+
+	tcpFd, err := getFD(tcpListener)
+	if err != nil {
+		return err
+	}
+
+	rights := unix.UnixRights(tcpFd)
+	err = unix.Sendmsg(unixFD, nil, rights, nil, 0)
+	if err != nil {
+		return err
+	}
+
+	return nil
+}
+
+// Request checks for the presence of a unix domain socket at `socketPath` and
+// opens a connection. The server side of the socket will immediately send a
+// file descriptor of a TCP socket over the unix domain socket. This file
+// descriptor is converted into a net.Listener and returned to the caller for
+// immediate use.
+//
+// During the time between socket handoff and startup of the new server,
+// requests to the socket will block. Requests will only fail if the client
+// timeout is shorter than the duration of the handoff period.
+//
+// If nothing is listening on the other end of the unix domain socket,
+// ErrNoHandoff is returned. Clients should check for this condition, and dial
+// the TCP socket themselves.
+func Request(socketPath string) (net.Listener, error) {
+	conn, err := net.Dial("unix", socketPath)
+	if err != nil {
+		return nil, fmt.Errorf("%w: %v", ErrNoHandoff, err)
+	}
+	defer conn.Close()
+	err = conn.SetDeadline(time.Now().Add(1 * time.Second))
+	if err != nil {
+		return nil, err
+	}
+
+	_, err = conn.Write([]byte(magicPacket))
+	if err != nil {
+		return nil, fmt.Errorf("%w: failed to send magic packet", err)
+	}
+
+	f, err := (conn.(*net.UnixConn)).File()
+	if err != nil {
+		return nil, fmt.Errorf("%w: fd not read", err)
+	}
+	defer f.Close()
+
+	b := make([]byte, unix.CmsgSpace(4))
+	//nolint:dogsled
+	_, _, _, _, err = unix.Recvmsg(int(f.Fd()), nil, b, 0)
+	if err != nil {
+		return nil, fmt.Errorf("%w: msg not received", err)
+	}
+
+	cmsgs, err := unix.ParseSocketControlMessage(b)
+	if err != nil {
+		return nil, fmt.Errorf("%w: control msg not parsed", err)
+	}
+	fds, err := unix.ParseUnixRights(&cmsgs[0])
+	if err != nil {
+		return nil, fmt.Errorf("%w: invalid unix rights", err)
+	}
+	fd := fds[0]
+
+	listenerFD := os.NewFile(uintptr(fd), "listener")
+	defer f.Close()
+
+	l, err := net.FileListener(listenerFD)
+	if err != nil {
+		return nil, fmt.Errorf("%w: failed to acquire new fd", err)
+	}
+
+	return l, nil
+}
+
+// ErrNoHandoff indicates that no handoff was performed.
+var ErrNoHandoff = errors.New("no handoff")
+
+func getFD(conn syscall.Conn) (fd int, err error) {
+	raw, err := conn.SyscallConn()
+	if err != nil {
+		return -1, err
+	}
+
+	err = raw.Control(func(ptr uintptr) {
+		fd = int(ptr)
+	})
+	return fd, err
+}
diff --git a/go/vt/servenv/grpc_server.go b/go/vt/servenv/grpc_server.go
index 3ad79dc3641..72e1ffff310 100644
--- a/go/vt/servenv/grpc_server.go
+++ b/go/vt/servenv/grpc_server.go
@@ -290,7 +290,7 @@ func serveGRPC() {
 
 	// listen on the port
 	log.Infof("Listening for gRPC calls on port %v", gRPCPort)
-	listener, err := net.Listen("tcp", net.JoinHostPort(gRPCBindAddress, strconv.Itoa(gRPCPort)))
+	listener, err := HandoffOrListen("grpc", "tcp", net.JoinHostPort(gRPCBindAddress, strconv.Itoa(gRPCPort)))
 	if err != nil {
 		log.Exitf("Cannot listen on port %v for gRPC: %v", gRPCPort, err)
 	}
diff --git a/go/vt/servenv/handoff.go b/go/vt/servenv/handoff.go
new file mode 100644
index 00000000000..99853478d1a
--- /dev/null
+++ b/go/vt/servenv/handoff.go
@@ -0,0 +1,85 @@
+/*
+Copyright 2025 The Vitess Authors.
+
+Licensed under the Apache License, Version 2.0 (the "License");
+you may not use this file except in compliance with the License.
+You may obtain a copy of the License at
+
+    http://www.apache.org/licenses/LICENSE-2.0
+
+Unless required by applicable law or agreed to in writing, software
+distributed under the License is distributed on an "AS IS" BASIS,
+WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+See the License for the specific language governing permissions and
+limitations under the License.
+*/
+
+package servenv
+
+import (
+	"errors"
+	"net"
+
+	"github.com/spf13/pflag"
+
+	"vitess.io/vitess/go/handoff"
+	"vitess.io/vitess/go/vt/log"
+)
+
+var (
+	// handoffPath specifies the filesystem path where handoff sockets are to be created,
+	// if zero-downtime handoff is enabled.
+	//
+	// To expose this flag, call RegisterHandoffFlags before ParseFlags.
+	rootHandoffPath string
+)
+
+func RegisterHandoffFlags() {
+	OnParse(func(fs *pflag.FlagSet) {
+		fs.StringVar(&rootHandoffPath, "handoff_path", rootHandoffPath, "Root path to enable zero-downtime handoff sockets.")
+	})
+}
+
+// HandoffOrListen implements optional support for zero-downtime socket handoff.
+//
+// If enabled by configuring a root path for the handoff, this first attempts to
+// take over the socket from a running process, otherwise this just calls the regular
+// net.Listen. Once it takes over the socket or creates a new one, it will also start
+// listening for requests to hand off the socket to future runs.
+func HandoffOrListen(serviceName, protocol, address string) (net.Listener, error) {
+
+	// If there is no path to handoff, then just pass through to the core net.listen.
+	if rootHandoffPath == "" {
+		return net.Listen(protocol, address)
+	}
+
+	handoffPath := rootHandoffPath + serviceName
+
+	// Request socket from an already running process, or start a new
+	// listener to serve requests on.
+	log.Infof("handoff: requesting handoff socket from %s", handoffPath)
+	listener, err := handoff.Request(handoffPath)
+	if err == nil {
+		log.Infof("handoff: received handoff from %s", handoffPath)
+	} else {
+		if errors.Is(err, handoff.ErrNoHandoff) {
+			log.Infof("handoff: no handoff, listening on %s %s", protocol, address)
+			listener, err = net.Listen(protocol, address)
+		} else {
+			log.Exitf("handoff: fatal error: %v", err)
+		}
+	}
+
+	// Advertise unix domain socket for handoff by future processes.
+	go func() {
+		err := handoff.Listen(handoffPath, listener)
+		if err != nil {
+			log.Errorf("Handoff failed: %v", err)
+			return
+		}
+
+		log.Infof("handed off socket %s %s", protocol, address)
+	}()
+
+	return listener, err
+}
diff --git a/go/vt/servenv/run.go b/go/vt/servenv/run.go
index 6f028786eaf..210158312cc 100644
--- a/go/vt/servenv/run.go
+++ b/go/vt/servenv/run.go
@@ -44,7 +44,7 @@ func Run(bindAddress string, port int) {
 	serveGRPC()
 	serveSocketFile()
 
-	l, err := net.Listen("tcp", net.JoinHostPort(bindAddress, strconv.Itoa(port)))
+	l, err := HandoffOrListen("servenv-"+strconv.Itoa(port), "tcp", net.JoinHostPort(bindAddress, strconv.Itoa(port)))
 	if err != nil {
 		log.Exit(err)
 	}
diff --git a/go/vt/vtgateproxy/mysql_server.go b/go/vt/vtgateproxy/mysql_server.go
index 65771400036..a988608dc53 100644
--- a/go/vt/vtgateproxy/mysql_server.go
+++ b/go/vt/vtgateproxy/mysql_server.go
@@ -30,6 +30,8 @@ import (
 	"syscall"
 	"time"
 
+	"github.com/pires/go-proxyproto"
+
 	"vitess.io/vitess/go/vt/sqlparser"
 	"vitess.io/vitess/go/vt/vtenv"
 	"vitess.io/vitess/go/vt/vterrors"
@@ -504,7 +506,15 @@ func initMySQLProtocol() {
 	}
 	if *mysqlServerPort >= 0 {
 		log.Infof("Mysql Server listening on Port %d", *mysqlServerPort)
-		mysqlListener, err = mysql.NewListener(*mysqlTCPVersion, net.JoinHostPort(*mysqlServerBindAddress, fmt.Sprintf("%v", *mysqlServerPort)), authServer, proxyHandle, *mysqlConnReadTimeout, *mysqlConnWriteTimeout, *mysqlProxyProtocol, *mysqlConnBufferPooling, *mysqlKeepAlivePeriod, *mysqlServerFlushDelay)
+		listener, err := servenv.HandoffOrListen("mysql", *mysqlTCPVersion, net.JoinHostPort(*mysqlServerBindAddress, fmt.Sprintf("%v", *mysqlServerPort)))
+		if err != nil {
+			log.Exitf("HandoffOrListen failed: %v", err)
+		}
+		if *mysqlProxyProtocol {
+			listener = &proxyproto.Listener{Listener: listener}
+		}
+
+		mysqlListener, err = mysql.NewFromListener(listener, authServer, proxyHandle, *mysqlConnReadTimeout, *mysqlConnWriteTimeout, *mysqlConnBufferPooling, *mysqlKeepAlivePeriod, *mysqlServerFlushDelay)
 		if err != nil {
 			log.Exitf("mysql.NewListener failed: %v", err)
 		}