diff --git a/coderd/coderd.go b/coderd/coderd.go
index 4603f78acc0d9..d11535f58022d 100644
--- a/coderd/coderd.go
+++ b/coderd/coderd.go
@@ -788,6 +788,7 @@ func New(options *Options) *API {
 		httpmw.AttachRequestID,
 		httpmw.ExtractRealIP(api.RealIPConfig),
 		httpmw.Logger(api.Logger),
+		singleSlashMW,
 		rolestore.CustomRoleMW,
 		prometheusMW,
 		// Build-Version is helpful for debugging.
@@ -1731,3 +1732,31 @@ func ReadExperiments(log slog.Logger, raw []string) codersdk.Experiments {
 	}
 	return exps
 }
+
+var multipleSlashesRe = regexp.MustCompile(`/+`)
+
+func singleSlashMW(next http.Handler) http.Handler {
+	fn := func(w http.ResponseWriter, r *http.Request) {
+		var path string
+		rctx := chi.RouteContext(r.Context())
+		if rctx != nil && rctx.RoutePath != "" {
+			path = rctx.RoutePath
+		} else {
+			path = r.URL.Path
+		}
+
+		// Normalize multiple slashes to a single slash
+		newPath := multipleSlashesRe.ReplaceAllString(path, "/")
+
+		// Apply the cleaned path
+		// The approach is consistent with: https://github.com/go-chi/chi/blob/e846b8304c769c4f1a51c9de06bebfaa4576bd88/middleware/strip.go#L24-L28
+		if rctx != nil {
+			rctx.RoutePath = newPath
+		} else {
+			r.URL.Path = newPath
+		}
+
+		next.ServeHTTP(w, r)
+	}
+	return http.HandlerFunc(fn)
+}
diff --git a/coderd/coderd_internal_test.go b/coderd/coderd_internal_test.go
new file mode 100644
index 0000000000000..34f5738bf90a0
--- /dev/null
+++ b/coderd/coderd_internal_test.go
@@ -0,0 +1,69 @@
+package coderd
+
+import (
+	"context"
+	"net/http"
+	"net/http/httptest"
+	"testing"
+
+	"github.com/go-chi/chi/v5"
+	"github.com/stretchr/testify/assert"
+)
+
+func TestStripSlashesMW(t *testing.T) {
+	t.Parallel()
+
+	tests := []struct {
+		name      string
+		inputPath string
+		wantPath  string
+	}{
+		{"No changes", "/api/v1/buildinfo", "/api/v1/buildinfo"},
+		{"Double slashes", "/api//v2//buildinfo", "/api/v2/buildinfo"},
+		{"Triple slashes", "/api///v2///buildinfo", "/api/v2/buildinfo"},
+		{"Leading slashes", "///api/v2/buildinfo", "/api/v2/buildinfo"},
+		{"Root path", "/", "/"},
+		{"Double slashes root", "//", "/"},
+		{"Only slashes", "/////", "/"},
+	}
+
+	handler := http.HandlerFunc(func(w http.ResponseWriter, _ *http.Request) {
+		w.WriteHeader(http.StatusOK)
+	})
+
+	for _, tt := range tests {
+		tt := tt
+
+		t.Run("chi/"+tt.name, func(t *testing.T) {
+			t.Parallel()
+			req := httptest.NewRequest("GET", tt.inputPath, nil)
+			rec := httptest.NewRecorder()
+
+			// given
+			rctx := chi.NewRouteContext()
+			rctx.RoutePath = tt.inputPath
+			req = req.WithContext(context.WithValue(req.Context(), chi.RouteCtxKey, rctx))
+
+			// when
+			singleSlashMW(handler).ServeHTTP(rec, req)
+			updatedCtx := chi.RouteContext(req.Context())
+
+			// then
+			assert.Equal(t, tt.inputPath, req.URL.Path)
+			assert.Equal(t, tt.wantPath, updatedCtx.RoutePath)
+		})
+
+		t.Run("stdlib/"+tt.name, func(t *testing.T) {
+			t.Parallel()
+			req := httptest.NewRequest("GET", tt.inputPath, nil)
+			rec := httptest.NewRecorder()
+
+			// when
+			singleSlashMW(handler).ServeHTTP(rec, req)
+
+			// then
+			assert.Equal(t, tt.wantPath, req.URL.Path)
+			assert.Nil(t, chi.RouteContext(req.Context()))
+		})
+	}
+}
diff --git a/site/vite.config.mts b/site/vite.config.mts
index 4deaac0dd5365..aab894ce0599e 100644
--- a/site/vite.config.mts
+++ b/site/vite.config.mts
@@ -52,6 +52,12 @@ export default defineConfig({
 				"csrf_token=JXm9hOUdZctWt0ZZGAy9xiS/gxMKYOThdxjjMnMUyn4=; Path=/; HttpOnly; SameSite=Lax",
 		},
 		proxy: {
+			"//": {
+				changeOrigin: true,
+				target: process.env.CODER_HOST || "http://localhost:3000",
+				secure: process.env.NODE_ENV === "production",
+				rewrite: (path) => path.replace(/\/+/g, "/"),
+			},
 			"/api": {
 				ws: true,
 				changeOrigin: true,