diff --git a/ipn/ipnlocal/cert.go b/ipn/ipnlocal/cert.go
index 8804fcb5c..b389c93e7 100644
--- a/ipn/ipnlocal/cert.go
+++ b/ipn/ipnlocal/cert.go
@@ -107,6 +107,15 @@ func (b *LocalBackend) GetCertPEM(ctx context.Context, domain string) (*TLSCertK
 // If a cert is expired, or expires sooner than minValidity, it will be renewed
 // synchronously. Otherwise it will be renewed asynchronously.
 func (b *LocalBackend) GetCertPEMWithValidity(ctx context.Context, domain string, minValidity time.Duration) (*TLSCertKeyPair, error) {
+	b.mu.Lock()
+	getCertForTest := b.getCertForTest
+	b.mu.Unlock()
+
+	if getCertForTest != nil {
+		testenv.AssertInTest()
+		return getCertForTest(domain)
+	}
+
 	if !validLookingCertDomain(domain) {
 		return nil, errors.New("invalid domain")
 	}
@@ -303,6 +312,16 @@ func (b *LocalBackend) getCertStore() (certStore, error) {
 	return certFileStore{dir: dir, testRoots: testX509Roots}, nil
 }
 
+// ConfigureCertsForTest sets a certificate retrieval function to be used by
+// this local backend, skipping the usual ACME certificate registration. Should
+// only be used in tests.
+func (b *LocalBackend) ConfigureCertsForTest(getCert func(hostname string) (*TLSCertKeyPair, error)) {
+	testenv.AssertInTest()
+	b.mu.Lock()
+	b.getCertForTest = getCert
+	b.mu.Unlock()
+}
+
 // certFileStore implements certStore by storing the cert & key files in the named directory.
 type certFileStore struct {
 	dir string
diff --git a/ipn/ipnlocal/local.go b/ipn/ipnlocal/local.go
index cebb96130..147be08eb 100644
--- a/ipn/ipnlocal/local.go
+++ b/ipn/ipnlocal/local.go
@@ -399,6 +399,10 @@ type LocalBackend struct {
 	// hardwareAttested is whether backend should use a hardware-backed key to
 	// bind the node identity to this device.
 	hardwareAttested atomic.Bool
+
+	// getCertForTest is used to retrieve TLS certificates in tests.
+	// See [LocalBackend.ConfigureCertsForTest].
+	getCertForTest func(hostname string) (*TLSCertKeyPair, error)
 }
 
 // SetHardwareAttested enables hardware attestation key signatures in map
diff --git a/tsnet/example/tsnet-services/tsnet-services.go b/tsnet/example/tsnet-services/tsnet-services.go
new file mode 100644
index 000000000..9aaa2ebba
--- /dev/null
+++ b/tsnet/example/tsnet-services/tsnet-services.go
@@ -0,0 +1,82 @@
+// Copyright (c) Tailscale Inc & AUTHORS
+// SPDX-License-Identifier: BSD-3-Clause
+
+// The tsnet-services example demonstrates how to use tsnet with Services.
+//
+// To run this example yourself:
+//
+//  1. Add access controls which (i) define a new ACL tag, (ii) allow the demo
+//     node to host the Service, and (iii) allow peers on the tailnet to reach
+//     the Service. A sample ACL policy is provided below.
+//
+//  2. Generate an auth key using the Tailscale admin panel. When doing so, add
+//     your new tag to your key (Service hosts must be tagged nodes).
+//
+//     https://tailscale.com/kb/1085/auth-keys#generate-an-auth-key
+//
+//  3. Define a Service. For the purposes of this demo, it must be defined to
+//     listen on TCP port 443. Note that you only need to follow Step 1 in the
+//     following document.
+//
+//     https://tailscale.com/kb/1552/tailscale-services#step-1-define-a-tailscale-service
+//
+//  4. Run the demo on the command line:
+//     TS_AUTHKEY=<yourkey> go run tsnet-services.go -service <service-name>
+//
+// Sample ACL policy for step 1:
+//
+//	"tagOwners": {
+//	   "tag:tsnet-demo-host": ["autogroup:member"],
+//	},
+//	"autoApprovers": {
+//	   "services": {
+//	      "svc:tsnet-demo": ["tag:tsnet-demo-host"],
+//	   },
+//	},
+//	"grants": [
+//	   "src": ["*"],
+//	   "dst": ["tag:tsnet-demo-host"],
+//	   "ip": ["*"],
+//	],
+package main
+
+import (
+	"flag"
+	"fmt"
+	"log"
+	"net/http"
+
+	"tailscale.com/tsnet"
+)
+
+var (
+	svcName = flag.String("service", "", "the name of your Service, e.g. svc:demo-service")
+)
+
+func main() {
+	flag.Parse()
+	if *svcName == "" {
+		log.Fatal("a Service name must be provided")
+	}
+
+	s := &tsnet.Server{
+		Hostname: "tsnet-services-demo",
+	}
+	defer s.Close()
+
+	ln, err := s.ListenService(*svcName, tsnet.ServiceModeHTTP{
+		HTTPS: true,
+		Port:  443,
+	})
+	if err != nil {
+		log.Fatal(err)
+	}
+	defer ln.Close()
+
+	log.Printf("Listening on https://%v\n", ln.FQDN)
+
+	err = http.Serve(ln, http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
+		fmt.Fprintln(w, "<html><body><h1>Hello, tailnet!</h1>")
+	}))
+	log.Fatal(err)
+}
diff --git a/tsnet/example_tsnet_listen_service_multiple_ports_test.go b/tsnet/example_tsnet_listen_service_multiple_ports_test.go
new file mode 100644
index 000000000..2b8f01526
--- /dev/null
+++ b/tsnet/example_tsnet_listen_service_multiple_ports_test.go
@@ -0,0 +1,66 @@
+package tsnet_test
+
+import (
+	"fmt"
+	"log"
+	"net/http"
+	_ "net/http/pprof"
+	"strings"
+
+	"tailscale.com/tsnet"
+)
+
+// This example function is in a separate file for the "net/http/pprof" import.
+
+// ExampleServer_ListenService_multiplePorts demonstrates how to advertise a
+// Service on multiple ports. In this example, we run an HTTPS server on 443 and
+// an HTTP server handling pprof requests to the same runtime on 6060.
+func ExampleServer_ListenService_multiplePorts() {
+	s := &tsnet.Server{
+		Hostname: "tsnet-services-demo",
+	}
+	defer s.Close()
+
+	ln, err := s.ListenService("svc:my-service", tsnet.ServiceModeHTTP{
+		HTTPS: true,
+		Port:  443,
+	})
+	if err != nil {
+		log.Fatal(err)
+	}
+	defer ln.Close()
+
+	pprofLn, err := s.ListenService("svc:my-service", tsnet.ServiceModeTCP{
+		Port: 6060,
+	})
+	if err != nil {
+		log.Fatal(err)
+	}
+	defer pprofLn.Close()
+
+	go func() {
+		log.Printf("Listening for pprof requests on http://%v:%d\n", pprofLn.FQDN, 6060)
+
+		handler := func(w http.ResponseWriter, r *http.Request) {
+			// The pprof listener is separate from our main server, so we can
+			// allow users to leave off the /debug/pprof prefix. We'll just
+			// attach it here, then pass along to the pprof handlers, which have
+			// been added implicitly due to our import of net/http/pprof.
+			if !strings.HasPrefix("/debug/pprof", r.URL.Path) {
+				r.URL.Path = "/debug/pprof" + r.URL.Path
+			}
+			http.DefaultServeMux.ServeHTTP(w, r)
+		}
+		if err := http.Serve(pprofLn, http.HandlerFunc(handler)); err != nil {
+			log.Fatal("error serving pprof:", err)
+		}
+	}()
+
+	log.Printf("Listening on https://%v\n", ln.FQDN)
+
+	// Specifying a handler here means pprof endpoints will not be served by
+	// this server (since we are not using http.DefaultServeMux).
+	log.Fatal(http.Serve(ln, http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
+		fmt.Fprintln(w, "<html><body><h1>Hello, tailnet!</h1>")
+	})))
+}
diff --git a/tsnet/example_tsnet_test.go b/tsnet/example_tsnet_test.go
index c5a20ab77..2a3236b3b 100644
--- a/tsnet/example_tsnet_test.go
+++ b/tsnet/example_tsnet_test.go
@@ -8,6 +8,8 @@ import (
 	"fmt"
 	"log"
 	"net/http"
+	"net/http/httputil"
+	"net/url"
 	"os"
 	"path/filepath"
 
@@ -200,3 +202,56 @@ func ExampleServer_ListenFunnel_funnelOnly() {
 		fmt.Fprintln(w, "Hi there! Welcome to the tailnet!")
 	})))
 }
+
+// ExampleServer_ListenService demonstrates how to advertise an HTTPS Service.
+func ExampleServer_ListenService() {
+	s := &tsnet.Server{
+		Hostname: "tsnet-services-demo",
+	}
+	defer s.Close()
+
+	ln, err := s.ListenService("svc:my-service", tsnet.ServiceModeHTTP{
+		HTTPS: true,
+		Port:  443,
+	})
+	if err != nil {
+		log.Fatal(err)
+	}
+	defer ln.Close()
+
+	log.Printf("Listening on https://%v\n", ln.FQDN)
+	log.Fatal(http.Serve(ln, http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
+		fmt.Fprintln(w, "<html><body><h1>Hello, tailnet!</h1>")
+	})))
+}
+
+// ExampleServer_ListenService_reverseProxy demonstrates how to advertise a
+// Service targeting a reverse proxy. This is useful when the backing server is
+// external to the tsnet application.
+func ExampleServer_ListenService_reverseProxy() {
+	// targetAddress represents the address of the backing server.
+	const targetAddress = "1.2.3.4:80"
+
+	// We will use a reverse proxy to direct traffic to the backing server.
+	reverseProxy := httputil.NewSingleHostReverseProxy(&url.URL{
+		Scheme: "http",
+		Host:   targetAddress,
+	})
+
+	s := &tsnet.Server{
+		Hostname: "tsnet-services-demo",
+	}
+	defer s.Close()
+
+	ln, err := s.ListenService("svc:my-service", tsnet.ServiceModeHTTP{
+		HTTPS: true,
+		Port:  443,
+	})
+	if err != nil {
+		log.Fatal(err)
+	}
+	defer ln.Close()
+
+	log.Printf("Listening on https://%v\n", ln.FQDN)
+	log.Fatal(http.Serve(ln, reverseProxy))
+}
diff --git a/tsnet/tsnet.go b/tsnet/tsnet.go
index 9efad32b3..fe353b58c 100644
--- a/tsnet/tsnet.go
+++ b/tsnet/tsnet.go
@@ -52,6 +52,7 @@ import (
 	"tailscale.com/net/proxymux"
 	"tailscale.com/net/socks5"
 	"tailscale.com/net/tsdial"
+	"tailscale.com/tailcfg"
 	"tailscale.com/tsd"
 	"tailscale.com/types/bools"
 	"tailscale.com/types/logger"
@@ -158,8 +159,6 @@ type Server struct {
 	// that the control server will allow the node to adopt that tag.
 	AdvertiseTags []string
 
-	getCertForTesting func(*tls.ClientHelloInfo) (*tls.Certificate, error)
-
 	initOnce             sync.Once
 	initErr              error
 	lb                   *ipnlocal.LocalBackend
@@ -1106,9 +1105,6 @@ func (s *Server) RegisterFallbackTCPHandler(cb FallbackTCPHandler) func() {
 // It calls GetCertificate on the localClient, passing in the ClientHelloInfo.
 // For testing, if s.getCertForTesting is set, it will call that instead.
 func (s *Server) getCert(hi *tls.ClientHelloInfo) (*tls.Certificate, error) {
-	if s.getCertForTesting != nil {
-		return s.getCertForTesting(hi)
-	}
 	lc, err := s.LocalClient()
 	if err != nil {
 		return nil, err
@@ -1259,6 +1255,266 @@ func (s *Server) ListenFunnel(network, addr string, opts ...FunnelOption) (net.L
 	return tls.NewListener(ln, tlsConfig), nil
 }
 
+// ServiceMode defines how a Service is run. Currently supported modes are:
+//   - [ServiceModeTCP]
+//   - [ServiceModeHTTP]
+//
+// For more information, see [Server.ListenService].
+type ServiceMode interface {
+	// serviceMode is a no-op used to identify a type as a ServiceMode.
+	serviceMode()
+
+	// network is the network this Service will advertise on. Per Go convention,
+	// this should be lowercase, e.g. 'tcp'.
+	network() string
+}
+
+// serviceModeWithPort is a convenience type to extract the port from
+// ServiceMode types which have one.
+type serviceModeWithPort interface {
+	ServiceMode
+	port() uint16
+}
+
+// ServiceModeTCP is used to configure a TCP Service via [Server.ListenService].
+type ServiceModeTCP struct {
+	// Port is the TCP port to advertise. If this Service needs to advertise
+	// multiple ports, call ListenService multiple times.
+	Port uint16
+
+	// TerminateTLS means that TLS connections will be terminated before being
+	// forwarded to the listener. In this case, the only server name indicator
+	// (SNI) permitted is the Service's fully-qualified domain name.
+	TerminateTLS bool
+
+	// PROXYProtocolVersion indicates whether to send a PROXY protocol header
+	// before forwarding the connection to the listener and which version of the
+	// protocol to use.
+	//
+	// For more information, see
+	// https://www.haproxy.org/download/1.8/doc/proxy-protocol.txt
+	PROXYProtocolVersion int
+}
+
+func (ServiceModeTCP) serviceMode() {}
+
+func (ServiceModeTCP) network() string { return "tcp" }
+
+func (m ServiceModeTCP) port() uint16 { return m.Port }
+
+// ServiceModeHTTP is used to configure an HTTP Service via
+// [Server.ListenService].
+type ServiceModeHTTP struct {
+	// Port is the TCP port to advertise. If this Service needs to advertise
+	// multiple ports, call ListenService multiple times.
+	Port uint16
+
+	// HTTPS, if true, means that the listener should handle connections as
+	// HTTPS connections. In this case, the only server name indicator (SNI)
+	// permitted is the Service's fully-qualified domain name.
+	HTTPS bool
+
+	// AcceptAppCaps defines the app capabilities to forward to the server. The
+	// keys in this map are the mount points for each set of capabilities.
+	//
+	// By example,
+	//
+	//  AcceptAppCaps: map[string][]string{
+	// 	  "/":    {"example.com/cap/all-paths"},
+	// 	  "/foo": {"example.com/cap/all-paths", "example.com/cap/foo"},
+	//  }
+	//
+	// would forward `example.com/cap/all-paths` to all paths on the server and
+	// `example.com/cap/foo` only to paths beginning with /foo.
+	//
+	// For more information on app capabilities, see
+	// https://tailscale.com/kb/1537/grants-app-capabilities
+	AcceptAppCaps map[string][]string
+
+	// PROXYProtocolVersion indicates whether to send a PROXY protocol header
+	// before forwarding the connection to the listener and which version of the
+	// protocol to use.
+	//
+	// For more information, see
+	// https://www.haproxy.org/download/1.8/doc/proxy-protocol.txt
+	PROXYProtocol int
+}
+
+func (ServiceModeHTTP) serviceMode() {}
+
+func (ServiceModeHTTP) network() string { return "tcp" }
+
+func (m ServiceModeHTTP) port() uint16 { return m.Port }
+
+func (m ServiceModeHTTP) capsMap() map[string][]tailcfg.PeerCapability {
+	capsMap := map[string][]tailcfg.PeerCapability{}
+	for path, capNames := range m.AcceptAppCaps {
+		caps := make([]tailcfg.PeerCapability, 0, len(capNames))
+		for _, c := range capNames {
+			caps = append(caps, tailcfg.PeerCapability(c))
+		}
+		capsMap[path] = caps
+	}
+	return capsMap
+}
+
+// A ServiceListener is a network listener for a Tailscale Service. For more
+// information about Services, see
+// https://tailscale.com/kb/1552/tailscale-services
+type ServiceListener struct {
+	net.Listener
+	addr addr
+
+	// FQDN is the fully-qualifed domain name of this Service.
+	FQDN string
+}
+
+// Addr returns the listener's network address. This will be the Service's
+// fully-qualified domain name (FQDN) and the port.
+//
+// A hostname is not truly a network address, but Services listen on multiple
+// addresses (the IPv4 and IPv6 virtual IPs).
+func (sl ServiceListener) Addr() net.Addr {
+	return sl.addr
+}
+
+// ErrUntaggedServiceHost is returned by ListenService when run on a node
+// without any ACL tags. A node must use a tag-based identity to act as a
+// Service host. For more information, see:
+// https://tailscale.com/kb/1552/tailscale-services#prerequisites
+var ErrUntaggedServiceHost = errors.New("service hosts must be tagged nodes")
+
+// ListenService creates a network listener for a Tailscale Service. This will
+// advertise this node as hosting the Service. Note that:
+//   - Approval must still be granted by an admin or by ACL auto-approval rules.
+//   - Service hosts must be tagged nodes.
+//   - A valid Service host must advertise all ports defined for the Service.
+//
+// To advertise a Service with multiple ports, run ListenService multiple times.
+// For more information about Services, see
+// https://tailscale.com/kb/1552/tailscale-services
+func (s *Server) ListenService(name string, mode ServiceMode) (*ServiceListener, error) {
+	if err := tailcfg.ServiceName(name).Validate(); err != nil {
+		return nil, err
+	}
+	if mode == nil {
+		return nil, errors.New("mode may not be nil")
+	}
+	svcName := name
+
+	// TODO(hwh33,tailscale/corp#35859): support TUN mode
+
+	ctx := context.Background()
+	_, err := s.Up(ctx)
+	if err != nil {
+		return nil, err
+	}
+
+	st := s.lb.StatusWithoutPeers()
+	if st.Self.Tags == nil || st.Self.Tags.Len() == 0 {
+		return nil, ErrUntaggedServiceHost
+	}
+
+	advertisedServices := s.lb.Prefs().AdvertiseServices().AsSlice()
+	if !slices.Contains(advertisedServices, svcName) {
+		// TODO(hwh33,tailscale/corp#35860): clean these prefs up when (a) we
+		// exit early due to error or (b) when the returned listener is closed.
+		_, err = s.lb.EditPrefs(&ipn.MaskedPrefs{
+			AdvertiseServicesSet: true,
+			Prefs: ipn.Prefs{
+				AdvertiseServices: append(advertisedServices, svcName),
+			},
+		})
+		if err != nil {
+			return nil, fmt.Errorf("updating advertised Services: %w", err)
+		}
+	}
+
+	srvConfig := new(ipn.ServeConfig)
+	sc, srvConfigETag, err := s.lb.ServeConfigETag()
+	if err != nil {
+		return nil, fmt.Errorf("fetching current serve config: %w", err)
+	}
+	if sc.Valid() {
+		srvConfig = sc.AsStruct()
+	}
+
+	fqdn := tailcfg.ServiceName(svcName).WithoutPrefix() + "." + st.CurrentTailnet.MagicDNSSuffix
+
+	// svcAddr is used to implement Addr() on the returned listener.
+	svcAddr := addr{
+		network: mode.network(),
+		// A hostname is not a network address, but Services listen on
+		// multiple addresses (the IPv4 and IPv6 virtual IPs), and there's
+		// no clear winner here between the two. Therefore prefer the FQDN.
+		//
+		// In the case of TCP or HTTP Services, the port will be added below.
+		addr: fqdn,
+	}
+	if m, ok := mode.(serviceModeWithPort); ok {
+		if m.port() == 0 {
+			return nil, errors.New("must specify a port to advertise")
+		}
+		svcAddr.addr += ":" + strconv.Itoa(int(m.port()))
+	}
+
+	// Start listening on a local TCP socket.
+	ln, err := net.Listen("tcp", "localhost:0")
+	if err != nil {
+		return nil, fmt.Errorf("starting local listener: %w", err)
+	}
+
+	switch m := mode.(type) {
+	case ServiceModeTCP:
+		// Forward all connections from service-hostname:port to our socket.
+		srvConfig.SetTCPForwardingForService(
+			m.Port, ln.Addr().String(), m.TerminateTLS,
+			tailcfg.ServiceName(svcName), m.PROXYProtocolVersion, st.CurrentTailnet.MagicDNSSuffix)
+	case ServiceModeHTTP:
+		// For HTTP Services, proxy all connections to our socket.
+		mds := st.CurrentTailnet.MagicDNSSuffix
+		haveRootHandler := false
+		// We need to add a separate proxy for each mount point in the caps map.
+		for path, caps := range m.capsMap() {
+			if !strings.HasPrefix(path, "/") {
+				path = "/" + path
+			}
+			h := ipn.HTTPHandler{
+				AcceptAppCaps: caps,
+				Proxy:         ln.Addr().String(),
+			}
+			if path == "/" {
+				haveRootHandler = true
+			} else {
+				h.Proxy += path
+			}
+			srvConfig.SetWebHandler(&h, svcName, m.Port, path, m.HTTPS, mds)
+		}
+		// We always need a root handler.
+		if !haveRootHandler {
+			h := ipn.HTTPHandler{Proxy: ln.Addr().String()}
+			srvConfig.SetWebHandler(&h, svcName, m.Port, "/", m.HTTPS, mds)
+		}
+	default:
+		ln.Close()
+		return nil, fmt.Errorf("unknown ServiceMode type %T", m)
+	}
+
+	if err := s.lb.SetServeConfig(srvConfig, srvConfigETag); err != nil {
+		ln.Close()
+		return nil, err
+	}
+
+	// TODO(hwh33,tailscale/corp#35860): clean up state (advertising prefs,
+	// serve config changes) when the returned listener is closed.
+
+	return &ServiceListener{
+		Listener: ln,
+		FQDN:     fqdn,
+		addr:     svcAddr,
+	}, nil
+}
+
 type listenOn string
 
 const (
@@ -1420,7 +1676,12 @@ func (ln *listener) Accept() (net.Conn, error) {
 	}
 }
 
-func (ln *listener) Addr() net.Addr { return addr{ln} }
+func (ln *listener) Addr() net.Addr {
+	return addr{
+		network: ln.keys[0].network,
+		addr:    ln.addr,
+	}
+}
 
 func (ln *listener) Close() error {
 	ln.s.mu.Lock()
@@ -1460,10 +1721,12 @@ func (ln *listener) handle(c net.Conn) {
 // Server returns the tsnet Server associated with the listener.
 func (ln *listener) Server() *Server { return ln.s }
 
-type addr struct{ ln *listener }
+type addr struct {
+	network, addr string
+}
 
-func (a addr) Network() string { return a.ln.keys[0].network }
-func (a addr) String() string  { return a.ln.addr }
+func (a addr) Network() string { return a.network }
+func (a addr) String() string  { return a.addr }
 
 // cleanupListener wraps a net.Listener with a function to be run on Close.
 type cleanupListener struct {
diff --git a/tsnet/tsnet_test.go b/tsnet/tsnet_test.go
index af8fa765d..93685993b 100644
--- a/tsnet/tsnet_test.go
+++ b/tsnet/tsnet_test.go
@@ -14,6 +14,7 @@ import (
 	"crypto/x509"
 	"crypto/x509/pkix"
 	"encoding/json"
+	"encoding/pem"
 	"errors"
 	"flag"
 	"fmt"
@@ -28,6 +29,7 @@ import (
 	"path/filepath"
 	"reflect"
 	"runtime"
+	"slices"
 	"strings"
 	"sync"
 	"sync/atomic"
@@ -38,10 +40,12 @@ import (
 	dto "github.com/prometheus/client_model/go"
 	"github.com/prometheus/common/expfmt"
 	"golang.org/x/net/proxy"
+
 	"tailscale.com/client/local"
 	"tailscale.com/cmd/testwrapper/flakytest"
 	"tailscale.com/internal/client/tailscale"
 	"tailscale.com/ipn"
+	"tailscale.com/ipn/ipnlocal"
 	"tailscale.com/ipn/store/mem"
 	"tailscale.com/net/netns"
 	"tailscale.com/tailcfg"
@@ -51,6 +55,8 @@ import (
 	"tailscale.com/tstest/integration/testcontrol"
 	"tailscale.com/types/key"
 	"tailscale.com/types/logger"
+	"tailscale.com/types/views"
+	"tailscale.com/util/mak"
 	"tailscale.com/util/must"
 )
 
@@ -136,7 +142,7 @@ func startControl(t *testing.T) (controlURL string, control *testcontrol.Server)
 
 type testCertIssuer struct {
 	mu    sync.Mutex
-	certs map[string]*tls.Certificate
+	certs map[string]ipnlocal.TLSCertKeyPair // keyed by hostname
 
 	root    *x509.Certificate
 	rootKey *ecdsa.PrivateKey
@@ -168,18 +174,18 @@ func newCertIssuer() *testCertIssuer {
 		panic(err)
 	}
 	return &testCertIssuer{
-		certs:   make(map[string]*tls.Certificate),
 		root:    rootCA,
 		rootKey: rootKey,
+		certs:   map[string]ipnlocal.TLSCertKeyPair{},
 	}
 }
 
-func (tci *testCertIssuer) getCert(chi *tls.ClientHelloInfo) (*tls.Certificate, error) {
+func (tci *testCertIssuer) getCert(hostname string) (*ipnlocal.TLSCertKeyPair, error) {
 	tci.mu.Lock()
 	defer tci.mu.Unlock()
-	cert, ok := tci.certs[chi.ServerName]
+	cert, ok := tci.certs[hostname]
 	if ok {
-		return cert, nil
+		return &cert, nil
 	}
 
 	certPrivKey, err := ecdsa.GenerateKey(elliptic.P256(), rand.Reader)
@@ -188,7 +194,7 @@ func (tci *testCertIssuer) getCert(chi *tls.ClientHelloInfo) (*tls.Certificate,
 	}
 	certTmpl := &x509.Certificate{
 		SerialNumber: big.NewInt(1),
-		DNSNames:     []string{chi.ServerName},
+		DNSNames:     []string{hostname},
 		NotBefore:    time.Now(),
 		NotAfter:     time.Now().Add(time.Hour),
 	}
@@ -196,12 +202,22 @@ func (tci *testCertIssuer) getCert(chi *tls.ClientHelloInfo) (*tls.Certificate,
 	if err != nil {
 		return nil, err
 	}
-	cert = &tls.Certificate{
-		Certificate: [][]byte{certDER, tci.root.Raw},
-		PrivateKey:  certPrivKey,
+	keyDER, err := x509.MarshalPKCS8PrivateKey(certPrivKey)
+	if err != nil {
+		return nil, err
 	}
-	tci.certs[chi.ServerName] = cert
-	return cert, nil
+	cert = ipnlocal.TLSCertKeyPair{
+		CertPEM: pem.EncodeToMemory(&pem.Block{
+			Type:  "CERTIFICATE",
+			Bytes: certDER,
+		}),
+		KeyPEM: pem.EncodeToMemory(&pem.Block{
+			Type:  "PRIVATE KEY",
+			Bytes: keyDER,
+		}),
+	}
+	tci.certs[hostname] = cert
+	return &cert, nil
 }
 
 func (tci *testCertIssuer) Pool() *x509.CertPool {
@@ -218,12 +234,11 @@ func startServer(t *testing.T, ctx context.Context, controlURL, hostname string)
 	tmp := filepath.Join(t.TempDir(), hostname)
 	os.MkdirAll(tmp, 0755)
 	s := &Server{
-		Dir:               tmp,
-		ControlURL:        controlURL,
-		Hostname:          hostname,
-		Store:             new(mem.Store),
-		Ephemeral:         true,
-		getCertForTesting: testCertRoot.getCert,
+		Dir:        tmp,
+		ControlURL: controlURL,
+		Hostname:   hostname,
+		Store:      new(mem.Store),
+		Ephemeral:  true,
 	}
 	if *verboseNodes {
 		s.Logf = t.Logf
@@ -234,6 +249,8 @@ func startServer(t *testing.T, ctx context.Context, controlURL, hostname string)
 	if err != nil {
 		t.Fatal(err)
 	}
+	s.lb.ConfigureCertsForTest(testCertRoot.getCert)
+
 	return s, status.TailscaleIPs[0], status.Self.PublicKey
 }
 
@@ -259,12 +276,11 @@ func TestDialBlocks(t *testing.T) {
 	tmp := filepath.Join(t.TempDir(), "s2")
 	os.MkdirAll(tmp, 0755)
 	s2 := &Server{
-		Dir:               tmp,
-		ControlURL:        controlURL,
-		Hostname:          "s2",
-		Store:             new(mem.Store),
-		Ephemeral:         true,
-		getCertForTesting: testCertRoot.getCert,
+		Dir:        tmp,
+		ControlURL: controlURL,
+		Hostname:   "s2",
+		Store:      new(mem.Store),
+		Ephemeral:  true,
 	}
 	if *verboseNodes {
 		s2.Logf = log.Printf
@@ -842,6 +858,366 @@ func TestFunnelClose(t *testing.T) {
 	})
 }
 
+func TestListenService(t *testing.T) {
+	// First test an error case which doesn't require all of the fancy setup.
+	t.Run("untagged_node_error", func(t *testing.T) {
+		ctx := t.Context()
+
+		controlURL, _ := startControl(t)
+		serviceHost, _, _ := startServer(t, ctx, controlURL, "service-host")
+
+		ln, err := serviceHost.ListenService("svc:foo", ServiceModeTCP{Port: 8080})
+		if ln != nil {
+			ln.Close()
+		}
+		if !errors.Is(err, ErrUntaggedServiceHost) {
+			t.Fatalf("expected %v, got %v", ErrUntaggedServiceHost, err)
+		}
+	})
+
+	// Now on to the fancier tests.
+
+	type dialFn func(context.Context, string, string) (net.Conn, error)
+
+	// TCP helpers
+	acceptAndEcho := func(t *testing.T, ln net.Listener) {
+		t.Helper()
+		conn, err := ln.Accept()
+		if err != nil {
+			t.Error("accept error:", err)
+			return
+		}
+		defer conn.Close()
+		if _, err := io.Copy(conn, conn); err != nil {
+			t.Error("copy error:", err)
+		}
+	}
+	assertEcho := func(t *testing.T, conn net.Conn) {
+		t.Helper()
+		msg := "echo"
+		buf := make([]byte, 1024)
+		if _, err := conn.Write([]byte(msg)); err != nil {
+			t.Fatal("write failed:", err)
+		}
+		n, err := conn.Read(buf)
+		if err != nil {
+			t.Fatal("read failed:", err)
+		}
+		got := string(buf[:n])
+		if got != msg {
+			t.Fatalf("unexpected response:\n\twant: %s\n\tgot: %s", msg, got)
+		}
+	}
+
+	// HTTP helpers
+	checkAndEcho := func(t *testing.T, ln net.Listener, check func(r *http.Request)) {
+		t.Helper()
+		if check == nil {
+			check = func(*http.Request) {}
+		}
+		http.Serve(ln, http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
+			defer r.Body.Close()
+			check(r)
+			if _, err := io.Copy(w, r.Body); err != nil {
+				t.Error("copy error:", err)
+				w.WriteHeader(http.StatusInternalServerError)
+			}
+		}))
+	}
+	assertEchoHTTP := func(t *testing.T, hostname, path string, dial dialFn) {
+		t.Helper()
+		c := http.Client{
+			Transport: &http.Transport{
+				DialContext: dial,
+			},
+		}
+		msg := "echo"
+		resp, err := c.Post("http://"+hostname+path, "text/plain", strings.NewReader(msg))
+		if err != nil {
+			t.Fatal("posting request:", err)
+		}
+		defer resp.Body.Close()
+		b, err := io.ReadAll(resp.Body)
+		if err != nil {
+			t.Fatal("reading body:", err)
+		}
+		got := string(b)
+		if got != msg {
+			t.Fatalf("unexpected response:\n\twant: %s\n\tgot: %s", msg, got)
+		}
+	}
+
+	tests := []struct {
+		name string
+
+		// modes is used as input to [Server.ListenService].
+		//
+		// If this slice has multiple modes, then ListenService will be invoked
+		// multiple times. The number of listeners provided to the run function
+		// (below) will always match the number of elements in this slice.
+		modes []ServiceMode
+
+		extraSetup func(t *testing.T, control *testcontrol.Server)
+
+		// run executes the test. This function does not need to close any of
+		// the input resources, but it should close any new resources it opens.
+		// listeners[i] corresponds to inputs[i].
+		run func(t *testing.T, listeners []*ServiceListener, peer *Server)
+	}{
+		{
+			name: "basic_TCP",
+			modes: []ServiceMode{
+				ServiceModeTCP{Port: 99},
+			},
+			run: func(t *testing.T, listeners []*ServiceListener, peer *Server) {
+				go acceptAndEcho(t, listeners[0])
+
+				target := fmt.Sprintf("%s:%d", listeners[0].FQDN, 99)
+				conn := must.Get(peer.Dial(t.Context(), "tcp", target))
+				defer conn.Close()
+
+				assertEcho(t, conn)
+			},
+		},
+		{
+			name: "TLS_terminated_TCP",
+			modes: []ServiceMode{
+				ServiceModeTCP{
+					TerminateTLS: true,
+					Port:         443,
+				},
+			},
+			run: func(t *testing.T, listeners []*ServiceListener, peer *Server) {
+				go acceptAndEcho(t, listeners[0])
+
+				target := fmt.Sprintf("%s:%d", listeners[0].FQDN, 443)
+				conn := must.Get(peer.Dial(t.Context(), "tcp", target))
+				defer conn.Close()
+
+				assertEcho(t, tls.Client(conn, &tls.Config{
+					ServerName: listeners[0].FQDN,
+					RootCAs:    testCertRoot.Pool(),
+				}))
+			},
+		},
+		{
+			name: "identity_headers",
+			modes: []ServiceMode{
+				ServiceModeHTTP{
+					Port: 80,
+				},
+			},
+			run: func(t *testing.T, listeners []*ServiceListener, peer *Server) {
+				expectHeader := "Tailscale-User-Name"
+				go checkAndEcho(t, listeners[0], func(r *http.Request) {
+					if _, ok := r.Header[expectHeader]; !ok {
+						t.Error("did not see expected header:", expectHeader)
+					}
+				})
+				assertEchoHTTP(t, listeners[0].FQDN, "", peer.Dial)
+			},
+		},
+		{
+			name: "identity_headers_TLS",
+			modes: []ServiceMode{
+				ServiceModeHTTP{
+					HTTPS: true,
+					Port:  80,
+				},
+			},
+			run: func(t *testing.T, listeners []*ServiceListener, peer *Server) {
+				expectHeader := "Tailscale-User-Name"
+				go checkAndEcho(t, listeners[0], func(r *http.Request) {
+					if _, ok := r.Header[expectHeader]; !ok {
+						t.Error("did not see expected header:", expectHeader)
+					}
+				})
+
+				dial := func(ctx context.Context, network, addr string) (net.Conn, error) {
+					tcpConn, err := peer.Dial(ctx, network, addr)
+					if err != nil {
+						return nil, err
+					}
+					return tls.Client(tcpConn, &tls.Config{
+						ServerName: listeners[0].FQDN,
+						RootCAs:    testCertRoot.Pool(),
+					}), nil
+				}
+
+				assertEchoHTTP(t, listeners[0].FQDN, "", dial)
+			},
+		},
+		{
+			name: "app_capabilities",
+			modes: []ServiceMode{
+				ServiceModeHTTP{
+					Port: 80,
+					AcceptAppCaps: map[string][]string{
+						"/":    {"example.com/cap/all-paths"},
+						"/foo": {"example.com/cap/all-paths", "example.com/cap/foo"},
+					},
+				},
+			},
+			extraSetup: func(t *testing.T, control *testcontrol.Server) {
+				control.SetGlobalAppCaps(tailcfg.PeerCapMap{
+					"example.com/cap/all-paths": []tailcfg.RawMessage{`true`},
+					"example.com/cap/foo":       []tailcfg.RawMessage{`true`},
+				})
+			},
+			run: func(t *testing.T, listeners []*ServiceListener, peer *Server) {
+				allPathsCap := "example.com/cap/all-paths"
+				fooCap := "example.com/cap/foo"
+				checkCaps := func(r *http.Request) {
+					rawCaps, ok := r.Header["Tailscale-App-Capabilities"]
+					if !ok {
+						t.Error("no app capabilities header")
+						return
+					}
+					if len(rawCaps) != 1 {
+						t.Error("expected one app capabilities header value, got", len(rawCaps))
+						return
+					}
+					var caps map[string][]any
+					if err := json.Unmarshal([]byte(rawCaps[0]), &caps); err != nil {
+						t.Error("error unmarshaling app caps:", err)
+						return
+					}
+					if _, ok := caps[allPathsCap]; !ok {
+						t.Errorf("got app caps, but %v is not present; saw:\n%v", allPathsCap, caps)
+					}
+					if strings.HasPrefix(r.URL.Path, "/foo") {
+						if _, ok := caps[fooCap]; !ok {
+							t.Errorf("%v should be present for /foo request; saw:\n%v", fooCap, caps)
+						}
+					} else {
+						if _, ok := caps[fooCap]; ok {
+							t.Errorf("%v should not be present for non-/foo request; saw:\n%v", fooCap, caps)
+						}
+					}
+				}
+
+				go checkAndEcho(t, listeners[0], checkCaps)
+				assertEchoHTTP(t, listeners[0].FQDN, "", peer.Dial)
+				assertEchoHTTP(t, listeners[0].FQDN, "/foo", peer.Dial)
+				assertEchoHTTP(t, listeners[0].FQDN, "/foo/bar", peer.Dial)
+			},
+		},
+		{
+			name: "multiple_ports",
+			modes: []ServiceMode{
+				ServiceModeTCP{
+					Port: 99,
+				},
+				ServiceModeHTTP{
+					Port: 80,
+				},
+			},
+			run: func(t *testing.T, listeners []*ServiceListener, peer *Server) {
+				go acceptAndEcho(t, listeners[0])
+
+				target := fmt.Sprintf("%s:%d", listeners[0].FQDN, 99)
+				conn := must.Get(peer.Dial(t.Context(), "tcp", target))
+				defer conn.Close()
+				assertEcho(t, conn)
+
+				go checkAndEcho(t, listeners[1], nil)
+				assertEchoHTTP(t, listeners[1].FQDN, "", peer.Dial)
+			},
+		},
+	}
+
+	for _, tt := range tests {
+		// Overview:
+		// - start test control
+		// - start 2 tsnet nodes:
+		//     one to act as Service host and a second to act as a peer client
+		// - configure necessary state on control mock
+		// - start a Service listener from the host
+		// - call tt.run with our test bed
+		//
+		// This ends up also testing the Service forwarding logic in
+		// LocalBackend, but that's useful too.
+		t.Run(tt.name, func(t *testing.T) {
+			ctx := t.Context()
+
+			controlURL, control := startControl(t)
+			serviceHost, _, _ := startServer(t, ctx, controlURL, "service-host")
+			serviceClient, _, _ := startServer(t, ctx, controlURL, "service-client")
+
+			const serviceName = tailcfg.ServiceName("svc:foo")
+			const serviceVIP = "100.11.22.33"
+
+			// == Set up necessary state in our mock ==
+
+			// The Service host must have the 'service-host' capability, which
+			// is a mapping from the Service name to the Service VIP.
+			var serviceHostCaps map[tailcfg.ServiceName]views.Slice[netip.Addr]
+			mak.Set(&serviceHostCaps, serviceName, views.SliceOf([]netip.Addr{netip.MustParseAddr(serviceVIP)}))
+			j := must.Get(json.Marshal(serviceHostCaps))
+			cm := serviceHost.lb.NetMap().SelfNode.CapMap().AsMap()
+			mak.Set(&cm, tailcfg.NodeAttrServiceHost, []tailcfg.RawMessage{tailcfg.RawMessage(j)})
+			control.SetNodeCapMap(serviceHost.lb.NodeKey(), cm)
+
+			// The Service host must be allowed to advertise the Service VIP.
+			control.SetSubnetRoutes(serviceHost.lb.NodeKey(), []netip.Prefix{
+				netip.MustParsePrefix(serviceVIP + `/32`),
+			})
+
+			// The Service host must be a tagged node (any tag will do).
+			serviceHostNode := control.Node(serviceHost.lb.NodeKey())
+			serviceHostNode.Tags = append(serviceHostNode.Tags, "some-tag")
+			control.UpdateNode(serviceHostNode)
+
+			// The service client must accept routes advertised by other nodes
+			// (RouteAll is equivalent to --accept-routes).
+			must.Get(serviceClient.localClient.EditPrefs(ctx, &ipn.MaskedPrefs{
+				RouteAllSet: true,
+				Prefs: ipn.Prefs{
+					RouteAll: true,
+				},
+			}))
+
+			// Set up DNS for our Service.
+			control.DNSConfig.ExtraRecords = append(control.DNSConfig.ExtraRecords, tailcfg.DNSRecord{
+				Name:  serviceName.WithoutPrefix() + "." + control.MagicDNSDomain,
+				Value: serviceVIP,
+			})
+
+			if tt.extraSetup != nil {
+				tt.extraSetup(t, control)
+			}
+
+			// Force netmap updates to avoid race conditions. The nodes need to
+			// see our control updates before we can start the test.
+			must.Do(control.ForceNetmapUpdates())
+			netmapUpToDate := func(s *Server) bool {
+				nm := s.lb.NetMap()
+				return slices.ContainsFunc(nm.DNS.ExtraRecords, func(r tailcfg.DNSRecord) bool {
+					return r.Value == serviceVIP
+				})
+			}
+			for !netmapUpToDate(serviceClient) {
+				time.Sleep(10 * time.Millisecond)
+			}
+			for !netmapUpToDate(serviceHost) {
+				time.Sleep(10 * time.Millisecond)
+			}
+
+			// == Done setting up mock state ==
+
+			// Start the Service listeners.
+			listeners := make([]*ServiceListener, 0, len(tt.modes))
+			for _, input := range tt.modes {
+				ln := must.Get(serviceHost.ListenService(serviceName.String(), input))
+				defer ln.Close()
+				listeners = append(listeners, ln)
+			}
+
+			tt.run(t, listeners, serviceClient)
+		})
+	}
+}
+
 func TestListenerClose(t *testing.T) {
 	tstest.Shard(t)
 	ctx := context.Background()
diff --git a/tstest/integration/testcontrol/testcontrol.go b/tstest/integration/testcontrol/testcontrol.go
index 19964c91f..7b5f5ffaf 100644
--- a/tstest/integration/testcontrol/testcontrol.go
+++ b/tstest/integration/testcontrol/testcontrol.go
@@ -110,6 +110,16 @@ type Server struct {
 	// nodeCapMaps overrides the capability map sent down to a client.
 	nodeCapMaps map[key.NodePublic]tailcfg.NodeCapMap
 
+	// globalAppCaps configures global app capabilities, equivalent to:
+	//	"grants": [
+	//	   {
+	//	     "src": ["*"],
+	//	     "dst": ["*"],
+	//	     "app": <contents of the input map>
+	//	   }
+	//	]
+	globalAppCaps tailcfg.PeerCapMap
+
 	// suppressAutoMapResponses is the set of nodes that should not be sent
 	// automatic map responses from serveMap. (They should only get manually sent ones)
 	suppressAutoMapResponses set.Set[key.NodePublic]
@@ -289,6 +299,40 @@ func (s *Server) addDebugMessage(nodeKeyDst key.NodePublic, msg any) bool {
 	return sendUpdate(oldUpdatesCh, updateDebugInjection)
 }
 
+// ForceNetmapUpdates issues updated netmaps to all connected nodes. It is an
+// error for a node to disconnect while this function runs. The intended use
+// case is ensuring that state changes propagate before running a test. This
+// function cannot guarantee that nodes have processed the issued updates, so
+// tests should confirm processing by querying the nodes. By example:
+//
+//	if err := s.ForceNetmapUpdates(); err != nil {
+//	     // handle error
+//	}
+//	for !expectedChangesPresent(node.NetMap()) {
+//	  time.Sleep(10 * time.Millisecond)
+//	}
+func (s *Server) ForceNetmapUpdates() error {
+	s.mu.Lock()
+	connectedNodes := map[key.NodePublic]*tailcfg.Node{}
+	for k, n := range s.nodes {
+		if _, ok := s.updates[n.ID]; ok {
+			connectedNodes[k] = n
+		}
+	}
+	s.mu.Unlock()
+
+	for k, n := range connectedNodes {
+		mr, err := s.MapResponse(&tailcfg.MapRequest{NodeKey: k})
+		if err != nil {
+			return fmt.Errorf("generating map response for %v (%v): %w", n.ID, n.Hostinfo.Hostname(), err)
+		}
+		if !s.addDebugMessage(k, mr) {
+			return fmt.Errorf("sending map response to %v (%v): update channel full or missing for node", n.ID, n.Hostinfo.Hostname())
+		}
+	}
+	return nil
+}
+
 // Mark the Node key of every node as expired
 func (s *Server) SetExpireAllNodes(expired bool) {
 	s.mu.Lock()
@@ -531,6 +575,21 @@ func (s *Server) SetNodeCapMap(nodeKey key.NodePublic, capMap tailcfg.NodeCapMap
 	s.updateLocked("SetNodeCapMap", s.nodeIDsLocked(0))
 }
 
+// SetGlobalAppCaps configures global app capabilities. This is equivalent to
+//
+//	"grants": [
+//	   {
+//	     "src": ["*"],
+//	     "dst": ["*"],
+//	     "app": <contents of the input map>
+//	   }
+//	]
+func (s *Server) SetGlobalAppCaps(appCaps tailcfg.PeerCapMap) {
+	s.mu.Lock()
+	s.globalAppCaps = appCaps
+	s.mu.Unlock()
+}
+
 // nodeIDsLocked returns the node IDs of all nodes in the server, except
 // for the node with the given ID.
 func (s *Server) nodeIDsLocked(except tailcfg.NodeID) []tailcfg.NodeID {
@@ -838,6 +897,9 @@ func (s *Server) serveRegister(w http.ResponseWriter, r *http.Request, mkey key.
 			CapMap:            capMap,
 			Capabilities:      slices.Collect(maps.Keys(capMap)),
 		}
+		if s.MagicDNSDomain != "" {
+			node.Name = node.Name + "." + s.MagicDNSDomain + "."
+		}
 		s.nodes[nk] = node
 	}
 	requireAuth := s.RequireAuth
@@ -1261,9 +1323,7 @@ func (s *Server) MapResponse(req *tailcfg.MapRequest) (res *tailcfg.MapResponse,
 	dns := s.DNSConfig
 	if dns != nil && s.MagicDNSDomain != "" {
 		dns = dns.Clone()
-		dns.CertDomains = []string{
-			node.Hostinfo.Hostname() + "." + s.MagicDNSDomain,
-		}
+		dns.CertDomains = append(dns.CertDomains, node.Hostinfo.Hostname()+"."+s.MagicDNSDomain)
 	}
 
 	res = &tailcfg.MapResponse{
@@ -1279,6 +1339,7 @@ func (s *Server) MapResponse(req *tailcfg.MapRequest) (res *tailcfg.MapResponse,
 	s.mu.Lock()
 	nodeMasqs := s.masquerades[node.Key]
 	jailed := maps.Clone(s.peerIsJailed[node.Key])
+	globalAppCaps := s.globalAppCaps
 	s.mu.Unlock()
 	for _, p := range s.AllNodes() {
 		if p.StableID == node.StableID {
@@ -1330,6 +1391,18 @@ func (s *Server) MapResponse(req *tailcfg.MapRequest) (res *tailcfg.MapResponse,
 		v6Prefix,
 	}
 
+	if globalAppCaps != nil {
+		res.PacketFilter = append(res.PacketFilter, tailcfg.FilterRule{
+			SrcIPs: []string{"*"},
+			CapGrant: []tailcfg.CapGrant{
+				{
+					Dsts:   []netip.Prefix{tsaddr.AllIPv4(), tsaddr.AllIPv6()},
+					CapMap: globalAppCaps,
+				},
+			},
+		})
+	}
+
 	// If the server is tracking TKA state, and there's a single TKA head,
 	// add it to the MapResponse.
 	if s.tkaStorage != nil {