diff --git a/pkg/upstream/file.go b/pkg/upstream/file.go
index 26b1c0b9..b88a855d 100644
--- a/pkg/upstream/file.go
+++ b/pkg/upstream/file.go
@@ -2,9 +2,12 @@ package upstream
 
 import (
 	"net/http"
+	"net/url"
 	"runtime"
 	"strings"
 
+	"github.com/oauth2-proxy/oauth2-proxy/v7/pkg/apis/options"
+
 	"github.com/oauth2-proxy/oauth2-proxy/v7/pkg/apis/middleware"
 )
 
@@ -12,22 +15,53 @@ const fileScheme = "file"
 
 // newFileServer creates a new fileServer that can serve requests
 // to a file system location.
-func newFileServer(id, path, fileSystemPath string) http.Handler {
+func newFileServer(upstream options.Upstream, fileSystemPath string) http.Handler {
+	handler := newFileServerForPath(fileSystemPath)
+
+	if upstream.RewriteTarget == "" {
+		// if the upstream does not have a rewrite target, strip off the Path prefix
+		// (so e.g. a request for /static/some-file.html looks for some-file.html
+		// relative to the fileSystemPath rather than static/some-file.html).
+		handler = http.StripPrefix(upstream.Path, handler)
+	} else {
+		// if the upstream *does* have a rewrite target then that means the target
+		// path relative to the fileSystemPath will be the one in the (rewritten)
+		// RequestURI.
+		handler = requestURIToURL(handler)
+	}
 	return &fileServer{
-		upstream: id,
-		handler:  newFileServerForPath(path, fileSystemPath),
+		upstream: upstream.ID,
+		handler:  handler,
 	}
 }
 
 // newFileServerForPath creates a http.Handler to serve files from the filesystem
-func newFileServerForPath(path string, filesystemPath string) http.Handler {
+func newFileServerForPath(filesystemPath string) http.Handler {
 	// Windows fileSSystemPath will be be prefixed with `/`, eg`/C:/...,
 	// if they were parsed by url.Parse`
 	if runtime.GOOS == "windows" {
 		filesystemPath = strings.TrimPrefix(filesystemPath, "/")
 	}
 
-	return http.StripPrefix(path, http.FileServer(http.Dir(filesystemPath)))
+	return http.FileServer(http.Dir(filesystemPath))
+}
+
+// requestURIToURL returns a Handler that replaces the URL in its request with
+// the result of parsing req.RequestURI.  This is necessary for file handlers
+// that have a rewrite target, since http.FileServer uses req.URL.Path when
+// looking for the target file, but the rewrite handler only updates the
+// RequestURI, leaving the original path in the URL.
+func requestURIToURL(handler http.Handler) http.Handler {
+	return http.HandlerFunc(func(rw http.ResponseWriter, req *http.Request) {
+		reqURL, err := url.ParseRequestURI(req.RequestURI)
+		if err != nil {
+			http.Error(rw, "500 Internal Server Error", http.StatusInternalServerError)
+			return
+		}
+
+		req.URL = reqURL
+		handler.ServeHTTP(rw, req)
+	})
 }
 
 // fileServer represents a single filesystem upstream proxy
diff --git a/pkg/upstream/file_test.go b/pkg/upstream/file_test.go
index 307ee24b..9763f6c6 100644
--- a/pkg/upstream/file_test.go
+++ b/pkg/upstream/file_test.go
@@ -7,6 +7,8 @@ import (
 	"net/http/httptest"
 	"os"
 
+	"github.com/oauth2-proxy/oauth2-proxy/v7/pkg/apis/options"
+
 	middlewareapi "github.com/oauth2-proxy/oauth2-proxy/v7/pkg/apis/middleware"
 	. "github.com/onsi/ginkgo/v2"
 	. "github.com/onsi/gomega"
@@ -31,8 +33,12 @@ var _ = Describe("File Server Suite", func() {
 		_, err := io.ReadFull(rand.Reader, idBytes)
 		Expect(err).ToNot(HaveOccurred())
 		id = string(idBytes)
+		upstream := options.Upstream{
+			ID:   id,
+			Path: "/files",
+		}
 
-		handler = newFileServer(id, "/files", filesDir)
+		handler = newFileServer(upstream, filesDir)
 	})
 
 	AfterEach(func() {
diff --git a/pkg/upstream/proxy.go b/pkg/upstream/proxy.go
index 8eaefc1a..74b0d02d 100644
--- a/pkg/upstream/proxy.go
+++ b/pkg/upstream/proxy.go
@@ -81,7 +81,7 @@ func (m *multiUpstreamProxy) registerStaticResponseHandler(upstream options.Upst
 // registerFileServer registers a new fileServer based on the configuration given.
 func (m *multiUpstreamProxy) registerFileServer(upstream options.Upstream, u *url.URL, writer pagewriter.Writer) error {
 	logger.Printf("mapping path %q => file system %q", upstream.Path, u.Path)
-	return m.registerHandler(upstream, newFileServer(upstream.ID, upstream.Path, u.Path), writer)
+	return m.registerHandler(upstream, newFileServer(upstream, u.Path), writer)
 }
 
 // registerHTTPUpstreamProxy registers a new httpUpstreamProxy based on the configuration given.