diff --git a/coderd/httpmw/csrf.go b/coderd/httpmw/csrf.go
index e868019bac23b..8cd043146c082 100644
--- a/coderd/httpmw/csrf.go
+++ b/coderd/httpmw/csrf.go
@@ -22,7 +22,9 @@ func CSRF(secureCookie bool) func(next http.Handler) http.Handler {
 		mw.SetBaseCookie(http.Cookie{Path: "/", HttpOnly: true, SameSite: http.SameSiteLaxMode, Secure: secureCookie})
 		mw.SetFailureHandler(http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
 			sessCookie, err := r.Cookie(codersdk.SessionTokenCookie)
-			if err == nil && r.Header.Get(codersdk.SessionTokenHeader) != sessCookie.Value {
+			if err == nil &&
+				r.Header.Get(codersdk.SessionTokenHeader) != "" &&
+				r.Header.Get(codersdk.SessionTokenHeader) != sessCookie.Value {
 				// If a user is using header authentication and cookie auth, but the values
 				// do not match, the cookie value takes priority.
 				// At the very least, return a more helpful error to the user.
diff --git a/coderd/httpmw/csrf_test.go b/coderd/httpmw/csrf_test.go
index 12c6afe825f75..03f2babb2961a 100644
--- a/coderd/httpmw/csrf_test.go
+++ b/coderd/httpmw/csrf_test.go
@@ -3,6 +3,7 @@ package httpmw_test
 import (
 	"context"
 	"net/http"
+	"net/http/httptest"
 	"testing"
 
 	"github.com/justinas/nosurf"
@@ -69,3 +70,77 @@ func TestCSRFExemptList(t *testing.T) {
 		})
 	}
 }
+
+// TestCSRFError verifies the error message returned to a user when CSRF
+// checks fail.
+//
+//nolint:bodyclose // Using httptest.Recorders
+func TestCSRFError(t *testing.T) {
+	t.Parallel()
+
+	// Hard coded matching CSRF values
+	const csrfCookieValue = "JXm9hOUdZctWt0ZZGAy9xiS/gxMKYOThdxjjMnMUyn4="
+	const csrfHeaderValue = "KNKvagCBEHZK7ihe2t7fj6VeJ0UyTDco1yVUJE8N06oNqxLu5Zx1vRxZbgfC0mJJgeGkVjgs08mgPbcWPBkZ1A=="
+	// Use a url with "/api" as the root, other routes bypass CSRF.
+	const urlPath = "https://coder.com/api/v2/hello"
+
+	var handler http.Handler = http.HandlerFunc(func(writer http.ResponseWriter, request *http.Request) {
+		writer.WriteHeader(http.StatusOK)
+	})
+	handler = httpmw.CSRF(false)(handler)
+
+	// Not testing the error case, just providing the example of things working
+	// to base the failure tests off of.
+	t.Run("ValidCSRF", func(t *testing.T) {
+		t.Parallel()
+
+		req, err := http.NewRequestWithContext(context.Background(), http.MethodPost, urlPath, nil)
+		require.NoError(t, err)
+
+		req.AddCookie(&http.Cookie{Name: codersdk.SessionTokenCookie, Value: "session_token_value"})
+		req.AddCookie(&http.Cookie{Name: nosurf.CookieName, Value: csrfCookieValue})
+		req.Header.Add(nosurf.HeaderName, csrfHeaderValue)
+
+		rec := httptest.NewRecorder()
+		handler.ServeHTTP(rec, req)
+		resp := rec.Result()
+		require.Equal(t, http.StatusOK, resp.StatusCode)
+	})
+
+	// The classic CSRF failure returns the generic error.
+	t.Run("MissingCSRFHeader", func(t *testing.T) {
+		t.Parallel()
+
+		req, err := http.NewRequestWithContext(context.Background(), http.MethodPost, urlPath, nil)
+		require.NoError(t, err)
+
+		req.AddCookie(&http.Cookie{Name: codersdk.SessionTokenCookie, Value: "session_token_value"})
+		req.AddCookie(&http.Cookie{Name: nosurf.CookieName, Value: csrfCookieValue})
+
+		rec := httptest.NewRecorder()
+		handler.ServeHTTP(rec, req)
+		resp := rec.Result()
+		require.Equal(t, http.StatusBadRequest, resp.StatusCode)
+		require.Contains(t, rec.Body.String(), "Something is wrong with your CSRF token.")
+	})
+
+	// Include the CSRF cookie, but not the CSRF header value.
+	// Including the 'codersdk.SessionTokenHeader' will bypass CSRF only if
+	// it matches the cookie. If it does not, we expect a more helpful error.
+	t.Run("MismatchedHeaderAndCookie", func(t *testing.T) {
+		t.Parallel()
+
+		req, err := http.NewRequestWithContext(context.Background(), http.MethodPost, urlPath, nil)
+		require.NoError(t, err)
+
+		req.AddCookie(&http.Cookie{Name: codersdk.SessionTokenCookie, Value: "session_token_value"})
+		req.AddCookie(&http.Cookie{Name: nosurf.CookieName, Value: csrfCookieValue})
+		req.Header.Add(codersdk.SessionTokenHeader, "mismatched_value")
+
+		rec := httptest.NewRecorder()
+		handler.ServeHTTP(rec, req)
+		resp := rec.Result()
+		require.Equal(t, http.StatusBadRequest, resp.StatusCode)
+		require.Contains(t, rec.Body.String(), "CSRF error encountered. Authentication via")
+	})
+}