diff --git a/ipn/ipnlocal/serve.go b/ipn/ipnlocal/serve.go
index 4d6055bbd..ef3de235a 100644
--- a/ipn/ipnlocal/serve.go
+++ b/ipn/ipnlocal/serve.go
@@ -25,6 +25,7 @@ import (
 	"net/url"
 	"os"
 	"path"
+	"regexp"
 	"slices"
 	"strconv"
 	"strings"
@@ -82,6 +83,17 @@ var ErrProxyToTailscaledSocket = errors.New("cannot proxy to tailscaled socket")
 
 var serveHTTPContextKey ctxkey.Key[*serveHTTPContext]
 
+// handleInvalidCharsRe matches any character that is not a word character, hyphen, underscore, or dot.
+var handleInvalidCharsRe = regexp.MustCompile(`[^\w\-_.]+`)
+
+// handelizeLogin converts a login name (e.g. "John.Doe@example.com") into a
+// lowercase handle with only word characters, hyphens, underscores, and dots.
+// It takes the local part before '@' and replaces invalid characters with '-'.
+func handelizeLogin(login string) string {
+	localPart := strings.Split(login, "@")[0]
+	return handleInvalidCharsRe.ReplaceAllString(strings.ToLower(localPart), "-")
+}
+
 type serveHTTPContext struct {
 	SrcAddr       netip.AddrPort
 	ForVIPService tailcfg.ServiceName // "" means local
@@ -1021,6 +1033,7 @@ func (b *LocalBackend) addTailscaleIdentityHeaders(r *httputil.ProxyRequest) {
 	// Clear any incoming values squatting in the headers.
 	r.Out.Header.Del("Tailscale-User-Login")
 	r.Out.Header.Del("Tailscale-User-Name")
+	r.Out.Header.Del("Tailscale-User-Handle")
 	r.Out.Header.Del("Tailscale-User-Profile-Pic")
 	r.Out.Header.Del("Tailscale-Funnel-Request")
 	r.Out.Header.Del("Tailscale-Headers-Info")
@@ -1044,6 +1057,7 @@ func (b *LocalBackend) addTailscaleIdentityHeaders(r *httputil.ProxyRequest) {
 	}
 	r.Out.Header.Set("Tailscale-User-Login", encTailscaleHeaderValue(user.LoginName))
 	r.Out.Header.Set("Tailscale-User-Name", encTailscaleHeaderValue(user.DisplayName))
+	r.Out.Header.Set("Tailscale-User-Handle", encTailscaleHeaderValue(handelizeLogin(user.LoginName)))
 	r.Out.Header.Set("Tailscale-User-Profile-Pic", user.ProfilePicURL)
 	r.Out.Header.Set("Tailscale-Headers-Info", "https://tailscale.com/s/serve-headers")
 }
diff --git a/ipn/ipnlocal/serve_test.go b/ipn/ipnlocal/serve_test.go
index 6ee2181a0..846502c73 100644
--- a/ipn/ipnlocal/serve_test.go
+++ b/ipn/ipnlocal/serve_test.go
@@ -751,6 +751,7 @@ func TestServeHTTPProxyHeaders(t *testing.T) {
 				{"X-Forwarded-For", "100.150.151.152"},
 				{"Tailscale-User-Login", "someone@example.com"},
 				{"Tailscale-User-Name", "Some One"},
+				{"Tailscale-User-Handle", "someone"},
 				{"Tailscale-User-Profile-Pic", "https://example.com/photo.jpg"},
 				{"Tailscale-Headers-Info", "https://tailscale.com/s/serve-headers"},
 			},
@@ -763,6 +764,7 @@ func TestServeHTTPProxyHeaders(t *testing.T) {
 				{"X-Forwarded-For", "100.150.151.153"},
 				{"Tailscale-User-Login", ""},
 				{"Tailscale-User-Name", ""},
+				{"Tailscale-User-Handle", ""},
 				{"Tailscale-User-Profile-Pic", ""},
 				{"Tailscale-Headers-Info", ""},
 			},
@@ -775,6 +777,7 @@ func TestServeHTTPProxyHeaders(t *testing.T) {
 				{"X-Forwarded-For", "100.160.161.162"},
 				{"Tailscale-User-Login", ""},
 				{"Tailscale-User-Name", ""},
+				{"Tailscale-User-Handle", ""},
 				{"Tailscale-User-Profile-Pic", ""},
 				{"Tailscale-Headers-Info", ""},
 			},
@@ -806,6 +809,33 @@ func TestServeHTTPProxyHeaders(t *testing.T) {
 	}
 }
 
+func TestHandelizeLogin(t *testing.T) {
+	tests := []struct {
+		in   string
+		want string
+	}{
+		{"someone@example.com", "someone"},
+		{"john.doe@example.com", "john.doe"},
+		{"John.Doe@example.com", "john.doe"},
+		{"john-doe@example.com", "john-doe"},
+		{"john_doe@example.com", "john_doe"},
+		{"john123@example.com", "john123"},
+		{"john+doe@example.com", "john-doe"},
+		{"john!#$doe@example.com", "john-doe"},
+		{"john doe@example.com", "john-doe"},
+		{"jöhn@example.com", "j-hn"},
+		{"someone", "someone"},
+		{"@example.com", ""},
+		{"John.Doe-Test_123@example.com", "john.doe-test_123"},
+	}
+	for _, tt := range tests {
+		got := handelizeLogin(tt.in)
+		if got != tt.want {
+			t.Errorf("handelizeLogin(%q) = %q, want %q", tt.in, got, tt.want)
+		}
+	}
+}
+
 func TestServeHTTPProxyGrantHeader(t *testing.T) {
 	b := newTestBackend(t)
 
@@ -891,6 +921,7 @@ func TestServeHTTPProxyGrantHeader(t *testing.T) {
 				{"X-Forwarded-For", "100.150.151.152"},
 				{"Tailscale-User-Login", "someone@example.com"},
 				{"Tailscale-User-Name", "Some One"},
+				{"Tailscale-User-Handle", "someone"},
 				{"Tailscale-User-Profile-Pic", "https://example.com/photo.jpg"},
 				{"Tailscale-Headers-Info", "https://tailscale.com/s/serve-headers"},
 				{"Tailscale-App-Capabilities", `{"example.com/cap/interesting":[{"role":"🐿"}]}`},
@@ -904,6 +935,7 @@ func TestServeHTTPProxyGrantHeader(t *testing.T) {
 				{"X-Forwarded-For", "100.150.151.153"},
 				{"Tailscale-User-Login", ""},
 				{"Tailscale-User-Name", ""},
+				{"Tailscale-User-Handle", ""},
 				{"Tailscale-User-Profile-Pic", ""},
 				{"Tailscale-Headers-Info", ""},
 				{"Tailscale-App-Capabilities", `{"example.com/cap/boring":[{"role":"Viewer"}]}`},
@@ -917,6 +949,7 @@ func TestServeHTTPProxyGrantHeader(t *testing.T) {
 				{"X-Forwarded-For", "100.160.161.162"},
 				{"Tailscale-User-Login", ""},
 				{"Tailscale-User-Name", ""},
+				{"Tailscale-User-Handle", ""},
 				{"Tailscale-User-Profile-Pic", ""},
 				{"Tailscale-Headers-Info", ""},
 				{"Tailscale-App-Capabilities", ""},