diff --git a/client/web/web.go b/client/web/web.go
index 6203b4c18..e9810ccd0 100644
--- a/client/web/web.go
+++ b/client/web/web.go
@@ -203,35 +203,9 @@ func NewServer(opts ServerOpts) (s *Server, err error) {
 	}
 	s.assetsHandler, s.assetsCleanup = assetsHandler(s.devMode)
 
-	var metric string // clientmetric to report on startup
-
-	// Create handler for "/api" requests with CSRF protection.
-	// We don't require secure cookies, since the web client is regularly used
-	// on network appliances that are served on local non-https URLs.
-	// The client is secured by limiting the interface it listens on,
-	// or by authenticating requests before they reach the web client.
-	csrfProtect := csrf.Protect(s.csrfKey(), csrf.Secure(false))
-
-	// signal to the CSRF middleware that the request is being served over
-	// plaintext HTTP to skip TLS-only header checks.
-	withSetPlaintext := func(h http.Handler) http.Handler {
-		return http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
-			r = csrf.PlaintextHTTPRequest(r)
-			h.ServeHTTP(w, r)
-		})
-	}
-
-	switch s.mode {
-	case LoginServerMode:
-		s.apiHandler = csrfProtect(withSetPlaintext(http.HandlerFunc(s.serveLoginAPI)))
-		metric = "web_login_client_initialization"
-	case ReadOnlyServerMode:
-		s.apiHandler = csrfProtect(withSetPlaintext(http.HandlerFunc(s.serveLoginAPI)))
-		metric = "web_readonly_client_initialization"
-	case ManageServerMode:
-		s.apiHandler = csrfProtect(withSetPlaintext(http.HandlerFunc(s.serveAPI)))
-		metric = "web_client_initialization"
-	}
+	var metric string
+	s.apiHandler, metric = s.modeAPIHandler(s.mode)
+	s.apiHandler = s.withCSRF(s.apiHandler)
 
 	// Don't block startup on reporting metric.
 	// Report in separate go routine with 5 second timeout.
@@ -244,6 +218,39 @@ func NewServer(opts ServerOpts) (s *Server, err error) {
 	return s, nil
 }
 
+func (s *Server) withCSRF(h http.Handler) http.Handler {
+	csrfProtect := csrf.Protect(s.csrfKey(), csrf.Secure(false))
+
+	// ref https://github.com/tailscale/tailscale/pull/14822
+	// signal to the CSRF middleware that the request is being served over
+	// plaintext HTTP to skip TLS-only header checks.
+	withSetPlaintext := func(h http.Handler) http.Handler {
+		return http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
+			r = csrf.PlaintextHTTPRequest(r)
+			h.ServeHTTP(w, r)
+		})
+	}
+
+	// NB: the order of the withSetPlaintext and csrfProtect calls is important
+	// to ensure that we signal to the CSRF middleware that the request is being
+	// served over plaintext HTTP and not over TLS as it presumes by default.
+	return withSetPlaintext(csrfProtect(h))
+}
+
+func (s *Server) modeAPIHandler(mode ServerMode) (http.Handler, string) {
+	switch mode {
+	case LoginServerMode:
+		return http.HandlerFunc(s.serveLoginAPI), "web_login_client_initialization"
+	case ReadOnlyServerMode:
+		return http.HandlerFunc(s.serveLoginAPI), "web_readonly_client_initialization"
+	case ManageServerMode:
+		return http.HandlerFunc(s.serveAPI), "web_client_initialization"
+	default: // invalid mode
+		log.Fatalf("invalid mode: %v", mode)
+	}
+	return nil, ""
+}
+
 func (s *Server) Shutdown() {
 	s.logf("web.Server: shutting down")
 	if s.assetsCleanup != nil {
diff --git a/client/web/web_test.go b/client/web/web_test.go
index b9242f6ac..291356260 100644
--- a/client/web/web_test.go
+++ b/client/web/web_test.go
@@ -11,6 +11,7 @@ import (
 	"fmt"
 	"io"
 	"net/http"
+	"net/http/cookiejar"
 	"net/http/httptest"
 	"net/netip"
 	"net/url"
@@ -20,6 +21,7 @@ import (
 	"time"
 
 	"github.com/google/go-cmp/cmp"
+	"github.com/gorilla/csrf"
 	"tailscale.com/client/local"
 	"tailscale.com/client/tailscale/apitype"
 	"tailscale.com/ipn"
@@ -1477,3 +1479,83 @@ func mockWaitAuthURL(_ context.Context, id string, src tailcfg.NodeID) (*tailcfg
 		return nil, errors.New("unknown id")
 	}
 }
+
+func TestCSRFProtect(t *testing.T) {
+	s := &Server{}
+
+	mux := http.NewServeMux()
+	mux.HandleFunc("GET /test/csrf-token", func(w http.ResponseWriter, r *http.Request) {
+		token := csrf.Token(r)
+		_, err := io.WriteString(w, token)
+		if err != nil {
+			t.Fatal(err)
+		}
+	})
+	mux.HandleFunc("POST /test/csrf-protected", func(w http.ResponseWriter, r *http.Request) {
+		_, err := io.WriteString(w, "ok")
+		if err != nil {
+			t.Fatal(err)
+		}
+	})
+	h := s.withCSRF(mux)
+	ser := httptest.NewServer(h)
+	defer ser.Close()
+
+	jar, err := cookiejar.New(nil)
+	if err != nil {
+		t.Fatalf("unable to construct cookie jar: %v", err)
+	}
+
+	client := ser.Client()
+	client.Jar = jar
+
+	// make GET request to populate cookie jar
+	resp, err := client.Get(ser.URL + "/test/csrf-token")
+	if err != nil {
+		t.Fatalf("unable to make request: %v", err)
+	}
+	defer resp.Body.Close()
+	if resp.StatusCode != http.StatusOK {
+		t.Fatalf("unexpected status: %v", resp.Status)
+	}
+	tokenBytes, err := io.ReadAll(resp.Body)
+	if err != nil {
+		t.Fatalf("unable to read body: %v", err)
+	}
+
+	csrfToken := strings.TrimSpace(string(tokenBytes))
+	if csrfToken == "" {
+		t.Fatal("empty csrf token")
+	}
+
+	// make a POST request without the CSRF header; ensure it fails
+	resp, err = client.Post(ser.URL+"/test/csrf-protected", "text/plain", nil)
+	if err != nil {
+		t.Fatalf("unable to make request: %v", err)
+	}
+	if resp.StatusCode != http.StatusForbidden {
+		t.Fatalf("unexpected status: %v", resp.Status)
+	}
+
+	// make a POST request with the CSRF header; ensure it succeeds
+	req, err := http.NewRequest("POST", ser.URL+"/test/csrf-protected", nil)
+	if err != nil {
+		t.Fatalf("error building request: %v", err)
+	}
+	req.Header.Set("X-CSRF-Token", csrfToken)
+	resp, err = client.Do(req)
+	if err != nil {
+		t.Fatalf("unable to make request: %v", err)
+	}
+	if resp.StatusCode != http.StatusOK {
+		t.Fatalf("unexpected status: %v", resp.Status)
+	}
+	defer resp.Body.Close()
+	out, err := io.ReadAll(resp.Body)
+	if err != nil {
+		t.Fatalf("unable to read body: %v", err)
+	}
+	if string(out) != "ok" {
+		t.Fatalf("unexpected body: %q", out)
+	}
+}