diff --git a/caddyconfig/httpcaddyfile/addresses_test.go b/caddyconfig/httpcaddyfile/addresses_test.go
index 232460d0f..1933b32e5 100644
--- a/caddyconfig/httpcaddyfile/addresses_test.go
+++ b/caddyconfig/httpcaddyfile/addresses_test.go
@@ -1,9 +1,24 @@
 package httpcaddyfile
 
 import (
+	"strings"
 	"testing"
 )
 
+func TestSystemdListenPlaceholderSurvivesAdaptation(t *testing.T) {
+	adapted := adaptCaddyfile(t, `{
+		auto_https off
+	}
+
+	http://localhost {
+		bind fd/{systemd.listen.web}
+		respond ok
+	}`)
+	if !strings.Contains(adapted, `"listen":["fd/{systemd.listen.web}"]`) {
+		t.Fatalf("adapted listener lost systemd placeholder: %s", adapted)
+	}
+}
+
 func TestParseAddress(t *testing.T) {
 	for i, test := range []struct {
 		input                    string
diff --git a/caddytest/integration/systemd_socket_activation_linux_test.go b/caddytest/integration/systemd_socket_activation_linux_test.go
new file mode 100644
index 000000000..94711c2f4
--- /dev/null
+++ b/caddytest/integration/systemd_socket_activation_linux_test.go
@@ -0,0 +1,236 @@
+// Copyright 2015 Matthew Holt and The Caddy 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.
+
+//go:build linux
+
+package integration
+
+import (
+	"context"
+	"crypto/tls"
+	"fmt"
+	"io"
+	"net"
+	"os"
+	"os/exec"
+	"strconv"
+	"strings"
+	"testing"
+	"time"
+
+	"github.com/caddyserver/caddy/v2"
+)
+
+const systemdListenHelper = "CADDY_SYSTEMD_LISTEN_HELPER"
+
+func TestSystemdListenFDIntegration(t *testing.T) {
+	if os.Getenv(systemdListenHelper) == "1" {
+		runSystemdListenFDHelper(t)
+		return
+	}
+
+	tcpListener, err := net.Listen("tcp4", "127.0.0.1:0")
+	if err != nil {
+		t.Fatal(err)
+	}
+	tcpFile, err := tcpListener.(*net.TCPListener).File()
+	if err != nil {
+		t.Fatal(err)
+	}
+	_ = tcpListener.Close()
+	defer tcpFile.Close()
+
+	udpConn, err := net.ListenUDP("udp4", &net.UDPAddr{IP: net.IPv4(127, 0, 0, 1)})
+	if err != nil {
+		t.Fatal(err)
+	}
+	udpFile, err := udpConn.File()
+	if err != nil {
+		t.Fatal(err)
+	}
+	_ = udpConn.Close()
+	defer udpFile.Close()
+
+	h3Conn, err := net.ListenUDP("udp4", &net.UDPAddr{IP: net.IPv4(127, 0, 0, 1)})
+	if err != nil {
+		t.Fatal(err)
+	}
+	h3File, err := h3Conn.File()
+	if err != nil {
+		t.Fatal(err)
+	}
+	_ = h3Conn.Close()
+	defer h3File.Close()
+
+	ctx, cancel := context.WithTimeout(context.Background(), 10*time.Second)
+	defer cancel()
+	cmd := exec.CommandContext(ctx, os.Args[0], "-test.run=^TestSystemdListenFDIntegration$", "-test.v")
+	cmd.ExtraFiles = []*os.File{tcpFile, udpFile, h3File}
+	cmd.Env = append(withoutSystemdListenEnv(os.Environ()),
+		systemdListenHelper+"=1",
+		"LISTEN_FDS=3",
+		"LISTEN_FDNAMES=web:dns:h3",
+	)
+	output, err := cmd.CombinedOutput()
+	if err != nil {
+		t.Fatalf("helper failed: %v\n%s", err, output)
+	}
+}
+
+func runSystemdListenFDHelper(t *testing.T) {
+	t.Setenv("LISTEN_PID", strconv.Itoa(os.Getpid()))
+	repl := caddy.NewReplacer()
+
+	stream := resolveSystemdListenAddress(t, repl, "fd/{systemd.listen.web}", "fd/3")
+	lnAny, err := stream.Listen(context.Background(), 0, net.ListenConfig{})
+	if err != nil {
+		t.Fatal(err)
+	}
+	ln, ok := lnAny.(net.Listener)
+	if !ok {
+		t.Fatalf("stream listener has type %T", lnAny)
+	}
+	defer ln.Close()
+	checkInheritedStream(t, ln)
+	if _, err := repl.ReplaceOrErr("fd/{systemd.listen.missing}", true, true); err == nil {
+		t.Fatal("unknown descriptor name did not fail replacement")
+	}
+
+	// The inherited descriptor mapping belongs to the process. Keep using the
+	// first valid snapshot even if later code changes the environment.
+	t.Setenv("LISTEN_FDNAMES", "changed")
+
+	datagram := resolveSystemdListenAddress(t, repl, "fdgram/{systemd.listen.dns}", "fdgram/4")
+	pcAny, err := datagram.Listen(context.Background(), 0, net.ListenConfig{})
+	if err != nil {
+		t.Fatal(err)
+	}
+	pc, ok := pcAny.(net.PacketConn)
+	if !ok {
+		t.Fatalf("datagram listener has type %T", pcAny)
+	}
+	defer pc.Close()
+	checkInheritedDatagram(t, pc)
+
+	h3 := resolveSystemdListenAddress(t, repl, "fdgram/{systemd.listen.h3}", "fdgram/5")
+	var tlsConfig *tls.Config
+	tlsConfig = &tls.Config{
+		GetConfigForClient: func(*tls.ClientHelloInfo) (*tls.Config, error) {
+			return tlsConfig, nil
+		},
+	}
+	quicListener, err := h3.ListenQUIC(context.Background(), 0, net.ListenConfig{}, caddy.ListenQUICOptions{
+		TLSConfig: tlsConfig,
+	})
+	if err != nil {
+		t.Fatal(err)
+	}
+	if err := quicListener.Close(); err != nil {
+		t.Fatal(err)
+	}
+	if err := quicListener.Close(); err != nil {
+		t.Fatal(err)
+	}
+}
+
+func resolveSystemdListenAddress(t *testing.T, repl *caddy.Replacer, input, want string) caddy.NetworkAddress {
+	t.Helper()
+	resolved, err := repl.ReplaceOrErr(input, true, true)
+	if err != nil {
+		t.Fatal(err)
+	}
+	if resolved != want {
+		t.Fatalf("resolved address = %q; want %q", resolved, want)
+	}
+	address, err := caddy.ParseNetworkAddress(resolved)
+	if err != nil {
+		t.Fatal(err)
+	}
+	return address
+}
+
+func checkInheritedStream(t *testing.T, ln net.Listener) {
+	t.Helper()
+	done := make(chan error, 1)
+	go func() {
+		conn, err := ln.Accept()
+		if err != nil {
+			done <- err
+			return
+		}
+		defer conn.Close()
+		buf := make([]byte, 4)
+		_, err = io.ReadFull(conn, buf)
+		if err == nil && string(buf) != "ping" {
+			err = fmt.Errorf("received %q; want ping", buf)
+		}
+		done <- err
+	}()
+
+	conn, err := net.DialTimeout("tcp", ln.Addr().String(), time.Second)
+	if err != nil {
+		t.Fatal(err)
+	}
+	_, err = conn.Write([]byte("ping"))
+	_ = conn.Close()
+	if err != nil {
+		t.Fatal(err)
+	}
+	select {
+	case err := <-done:
+		if err != nil {
+			t.Fatal(err)
+		}
+	case <-time.After(time.Second):
+		t.Fatal("timed out waiting for inherited listener")
+	}
+}
+
+func checkInheritedDatagram(t *testing.T, pc net.PacketConn) {
+	t.Helper()
+	conn, err := net.Dial("udp", pc.LocalAddr().String())
+	if err != nil {
+		t.Fatal(err)
+	}
+	defer conn.Close()
+	if _, err := conn.Write([]byte("ping")); err != nil {
+		t.Fatal(err)
+	}
+	if err := pc.SetReadDeadline(time.Now().Add(time.Second)); err != nil {
+		t.Fatal(err)
+	}
+	buf := make([]byte, 4)
+	n, _, err := pc.ReadFrom(buf)
+	if err != nil {
+		t.Fatal(err)
+	}
+	if string(buf[:n]) != "ping" {
+		t.Fatalf("received %q; want ping", buf[:n])
+	}
+}
+
+func withoutSystemdListenEnv(env []string) []string {
+	filtered := make([]string, 0, len(env))
+	for _, entry := range env {
+		if strings.HasPrefix(entry, "LISTEN_PID=") ||
+			strings.HasPrefix(entry, "LISTEN_PIDFDID=") ||
+			strings.HasPrefix(entry, "LISTEN_FDS=") ||
+			strings.HasPrefix(entry, "LISTEN_FDNAMES=") ||
+			strings.HasPrefix(entry, systemdListenHelper+"=") {
+			continue
+		}
+		filtered = append(filtered, entry)
+	}
+	return filtered
+}
diff --git a/internal/systemd/listen.go b/internal/systemd/listen.go
new file mode 100644
index 000000000..ac4f26125
--- /dev/null
+++ b/internal/systemd/listen.go
@@ -0,0 +1,94 @@
+// Copyright 2015 Matthew Holt and The Caddy 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 systemd
+
+import (
+	"errors"
+	"fmt"
+	"math"
+	"os"
+	"strconv"
+	"strings"
+	"sync"
+)
+
+const systemdListenFDStart = 3 // stdin, stdout and stderr occupy descriptors 0 to 2
+
+var cachedSystemdListenFDs = sync.OnceValues(func() (map[string]int, error) {
+	return parseSystemdListenFDs(os.Getpid(), os.LookupEnv)
+})
+
+// ListenFD returns the first inherited descriptor with name.
+func ListenFD(name string) (int, error) {
+	descriptors, err := cachedSystemdListenFDs()
+	if err != nil {
+		return 0, err
+	}
+	return systemdListenFDByName(descriptors, name)
+}
+
+func parseSystemdListenFDs(pid int, lookupEnv func(string) (string, bool)) (map[string]int, error) {
+	listenPID, ok := lookupEnv("LISTEN_PID")
+	if !ok {
+		return nil, errors.New("systemd socket activation: LISTEN_PID is unset")
+	}
+	parsedPID, err := strconv.Atoi(listenPID)
+	if err != nil {
+		return nil, fmt.Errorf("systemd socket activation: parsing LISTEN_PID: %w", err)
+	}
+	if parsedPID != pid {
+		return nil, fmt.Errorf("systemd socket activation: LISTEN_PID does not match process: %d != %d", parsedPID, pid)
+	}
+
+	listenFDs, ok := lookupEnv("LISTEN_FDS")
+	if !ok {
+		return nil, errors.New("systemd socket activation: LISTEN_FDS is unset")
+	}
+	fdCount, err := strconv.Atoi(listenFDs)
+	if err != nil {
+		return nil, fmt.Errorf("systemd socket activation: parsing LISTEN_FDS: %w", err)
+	}
+	if fdCount <= 0 || fdCount > math.MaxInt-systemdListenFDStart {
+		return nil, fmt.Errorf("systemd socket activation: invalid LISTEN_FDS count: %d", fdCount)
+	}
+
+	listenFDNames, ok := lookupEnv("LISTEN_FDNAMES")
+	if !ok {
+		return nil, errors.New("systemd socket activation: LISTEN_FDNAMES is unset")
+	}
+	names := strings.Split(listenFDNames, ":")
+	if len(names) != fdCount {
+		return nil, fmt.Errorf("systemd socket activation: LISTEN_FDS does not match LISTEN_FDNAMES count: %d != %d", fdCount, len(names))
+	}
+
+	descriptors := make(map[string]int, len(names))
+	for index, name := range names {
+		if _, exists := descriptors[name]; !exists {
+			descriptors[name] = systemdListenFDStart + index
+		}
+	}
+	return descriptors, nil
+}
+
+func systemdListenFDByName(descriptors map[string]int, name string) (int, error) {
+	if name == "" {
+		return 0, errors.New("systemd listen descriptor name is empty")
+	}
+	descriptor, ok := descriptors[name]
+	if !ok {
+		return 0, fmt.Errorf("systemd listen descriptor name not found: %q", name)
+	}
+	return descriptor, nil
+}
diff --git a/internal/systemd/listen_test.go b/internal/systemd/listen_test.go
new file mode 100644
index 000000000..b3e0e8bfe
--- /dev/null
+++ b/internal/systemd/listen_test.go
@@ -0,0 +1,111 @@
+// Copyright 2015 Matthew Holt and The Caddy 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 systemd
+
+import (
+	"maps"
+	"testing"
+)
+
+func TestParseSystemdListenFDs(t *testing.T) {
+	for _, tc := range []struct {
+		name    string
+		pid     int
+		env     map[string]string
+		want    map[string]int
+		wantErr bool
+	}{
+		{
+			name: "named descriptors including duplicates",
+			pid:  42,
+			env: map[string]string{
+				"LISTEN_PID":     "42",
+				"LISTEN_FDS":     "5",
+				"LISTEN_FDNAMES": "web:dns:web:admin:web.api",
+			},
+			want: map[string]int{
+				"web":     3,
+				"dns":     4,
+				"admin":   6,
+				"web.api": 7,
+			},
+		},
+		{name: "missing pid", pid: 42, env: map[string]string{}, wantErr: true},
+		{name: "malformed pid", pid: 42, env: map[string]string{"LISTEN_PID": "x"}, wantErr: true},
+		{name: "different pid", pid: 42, env: map[string]string{"LISTEN_PID": "41"}, wantErr: true},
+		{name: "missing descriptor count", pid: 42, env: map[string]string{"LISTEN_PID": "42"}, wantErr: true},
+		{name: "zero descriptors", pid: 42, env: map[string]string{"LISTEN_PID": "42", "LISTEN_FDS": "0"}, wantErr: true},
+		{name: "negative descriptor count", pid: 42, env: map[string]string{"LISTEN_PID": "42", "LISTEN_FDS": "-1"}, wantErr: true},
+		{name: "missing names", pid: 42, env: map[string]string{"LISTEN_PID": "42", "LISTEN_FDS": "1"}, wantErr: true},
+		{name: "too few names", pid: 42, env: map[string]string{"LISTEN_PID": "42", "LISTEN_FDS": "2", "LISTEN_FDNAMES": "web"}, wantErr: true},
+		{name: "too many names", pid: 42, env: map[string]string{"LISTEN_PID": "42", "LISTEN_FDS": "1", "LISTEN_FDNAMES": "web:dns"}, wantErr: true},
+	} {
+		t.Run(tc.name, func(t *testing.T) {
+			got, err := parseSystemdListenFDs(tc.pid, func(name string) (string, bool) {
+				value, ok := tc.env[name]
+				return value, ok
+			})
+			if tc.wantErr {
+				if err == nil {
+					t.Fatal("expected an error")
+				}
+				return
+			}
+			if err != nil {
+				t.Fatal(err)
+			}
+			if !maps.Equal(got, tc.want) {
+				t.Fatalf("descriptor mapping = %#v; want %#v", got, tc.want)
+			}
+		})
+	}
+}
+
+func TestSystemdListenFDByName(t *testing.T) {
+	descriptors := map[string]int{
+		"web":     3,
+		"dns":     4,
+		"web.api": 5,
+	}
+
+	for _, tc := range []struct {
+		input   string
+		want    int
+		wantErr bool
+	}{
+		{input: "web", want: 3},
+		{input: "dns", want: 4},
+		{input: "web.api", want: 5},
+		{input: "", wantErr: true},
+		{input: "missing", wantErr: true},
+		{input: "web:1", wantErr: true},
+	} {
+		t.Run(tc.input, func(t *testing.T) {
+			got, err := systemdListenFDByName(descriptors, tc.input)
+			if tc.wantErr {
+				if err == nil {
+					t.Fatal("expected an error")
+				}
+				return
+			}
+			if err != nil {
+				t.Fatal(err)
+			}
+			if got != tc.want {
+				t.Fatalf("descriptor = %d; want %d", got, tc.want)
+			}
+		})
+	}
+}
diff --git a/replacer.go b/replacer.go
index 7a324165d..85d86cfc2 100644
--- a/replacer.go
+++ b/replacer.go
@@ -29,6 +29,8 @@ import (
 	"time"
 
 	"go.uber.org/zap"
+
+	"github.com/caddyserver/caddy/v2/internal/systemd"
 )
 
 // NewReplacer returns a new Replacer.
@@ -460,6 +462,13 @@ func (f globalDefaultReplacementProvider) replace(key string) (any, bool) {
 	if strings.HasPrefix(key, envPrefix) {
 		return os.Getenv(key[len(envPrefix):]), true
 	}
+	if name, ok := strings.CutPrefix(key, systemdListenPrefix); ok {
+		descriptor, err := systemd.ListenFD(name)
+		if err != nil {
+			return nil, false
+		}
+		return descriptor, true
+	}
 
 	switch key {
 	case "system.hostname":
@@ -531,5 +540,7 @@ const phOpen, phClose, phEscape = '{', '}', '\\'
 
 const filePrefix = "file."
 
+const systemdListenPrefix = "systemd.listen."
+
 // maxFileCacheBytes bounds the memoized file contents to 8 MiB (8,388,608 bytes) per replace call.
 const maxFileCacheBytes = 8 << 20