diff --git a/gitindex/index.go b/gitindex/index.go
index 183c3249..b6105ef8 100644
--- a/gitindex/index.go
+++ b/gitindex/index.go
@@ -32,6 +32,9 @@ import (
 	"strconv"
 	"strings"
 
+	"github.com/go-git/go-billy/v5/osfs"
+	"github.com/go-git/go-git/v5/plumbing/cache"
+	"github.com/go-git/go-git/v5/storage/filesystem"
 	"github.com/sourcegraph/zoekt"
 	"github.com/sourcegraph/zoekt/build"
 	"github.com/sourcegraph/zoekt/ignore"
@@ -404,10 +407,12 @@ func indexGitRepo(opts Options, config gitIndexConfig) (bool, error) {
 	}
 
 	opts.BuildOptions.RepositoryDescription.Source = opts.RepoDir
-	repo, err := git.PlainOpen(opts.RepoDir)
+
+	repo, repoCloser, err := openRepo(opts.RepoDir)
 	if err != nil {
-		return false, fmt.Errorf("git.PlainOpen: %w", err)
+		return false, fmt.Errorf("openRepo: %w", err)
 	}
+	defer repoCloser.Close()
 
 	if err := setTemplatesFromConfig(&opts.BuildOptions.RepositoryDescription, opts.RepoDir); err != nil {
 		log.Printf("setTemplatesFromConfig(%s): %s", opts.RepoDir, err)
@@ -572,6 +577,37 @@ func indexGitRepo(opts Options, config gitIndexConfig) (bool, error) {
 	return true, builder.Finish()
 }
 
+// openRepo opens a git repository in a way that's optimized for indexing.
+//
+// It copies the relevant logic from git.PlainOpen, and enables the filesystem KeepDescriptors option. This
+// caches the packfile handles, preventing the packfile from being opened then closed on every object access.
+func openRepo(repoDir string) (*git.Repository, io.Closer, error) {
+	fs := osfs.New(repoDir)
+
+	// Check if the root directory exists.
+	if _, err := fs.Stat(""); err != nil {
+		if os.IsNotExist(err) {
+			return nil, nil, git.ErrRepositoryNotExists
+		}
+		return nil, nil, err
+	}
+
+	// If there's a .git directory, use that as the new root.
+	if _, err := fs.Stat(git.GitDirName); err == nil {
+		if fs, err = fs.Chroot(git.GitDirName); err != nil {
+			return nil, nil, fmt.Errorf("fs.Chroot: %w", err)
+		}
+	}
+
+	s := filesystem.NewStorageWithOptions(fs, cache.NewObjectLRUDefault(), filesystem.Options{
+		KeepDescriptors: true,
+	})
+
+	// Because we're keeping descriptors open, we need to close the storage object when we're done.
+	repo, err := git.Open(s, fs)
+	return repo, s, err
+}
+
 type repoPathRanks struct {
 	MeanRank float64            `json:"mean_reference_count"`
 	Paths    map[string]float64 `json:"paths"`
diff --git a/gitindex/index_test.go b/gitindex/index_test.go
index d38b49f0..f655c960 100644
--- a/gitindex/index_test.go
+++ b/gitindex/index_test.go
@@ -17,6 +17,7 @@ package gitindex
 import (
 	"bytes"
 	"context"
+	"errors"
 	"fmt"
 	"net/url"
 	"os"
@@ -64,6 +65,83 @@ func TestIndexEmptyRepo(t *testing.T) {
 	}
 }
 
+func TestIndexNonexistentRepo(t *testing.T) {
+	dir := t.TempDir()
+	desc := zoekt.Repository{
+		Name: "nonexistent",
+	}
+	opts := Options{
+		RepoDir:  "does/not/exist",
+		Branches: []string{"main"},
+		BuildOptions: build.Options{
+			RepositoryDescription: desc,
+			IndexDir:              dir,
+		},
+	}
+
+	if _, err := IndexGitRepo(opts); err == nil {
+		t.Fatal("expected error, got none")
+	} else if !errors.Is(err, git.ErrRepositoryNotExists) {
+		t.Fatalf("expected git.ErrRepositoryNotExists, got %v", err)
+	}
+}
+
+func TestIndexTinyRepo(t *testing.T) {
+	// Create a repo with one file in it.
+	dir := t.TempDir()
+	executeCommand(t, dir, exec.Command("git", "init", "-b", "main", "repo"))
+	executeCommand(t, dir, exec.Command("git", "config", "--global", "user.name", "Thomas"))
+	executeCommand(t, dir, exec.Command("git", "config", "--global", "user.email", "thomas@google.com"))
+
+	if err := os.WriteFile(filepath.Join(dir, "repo", "file1.go"), []byte("package main\n\nfunc main() {}\n"), 0644); err != nil {
+		t.Fatalf("WriteFile: %v", err)
+	}
+
+	repoDir := filepath.Join(dir, "repo")
+	executeCommand(t, repoDir, exec.Command("git", "add", "."))
+	executeCommand(t, repoDir, exec.Command("git", "commit", "-m", "initial commit"))
+
+	// Test that indexing accepts both the repo directory, and the .git subdirectory.
+	for _, testDir := range []string{"repo", "repo/.git"} {
+		opts := Options{
+			RepoDir:  filepath.Join(dir, testDir),
+			Branches: []string{"main"},
+			BuildOptions: build.Options{
+				RepositoryDescription: zoekt.Repository{Name: "repo"},
+				IndexDir:              dir,
+			},
+		}
+
+		if _, err := IndexGitRepo(opts); err != nil {
+			t.Fatalf("unexpected error %v", err)
+		}
+
+		searcher, err := shards.NewDirectorySearcher(dir)
+		if err != nil {
+			t.Fatal("NewDirectorySearcher", err)
+		}
+
+		results, err := searcher.Search(context.Background(), &query.Const{Value: true}, &zoekt.SearchOptions{})
+		searcher.Close()
+
+		if err != nil {
+			t.Fatal("search failed", err)
+		}
+
+		if len(results.Files) != 1 {
+			t.Fatalf("got search result %v, want 1 file", results.Files)
+		}
+	}
+}
+
+func executeCommand(t *testing.T, dir string, cmd *exec.Cmd) *exec.Cmd {
+	cmd.Dir = dir
+	if err := cmd.Run(); err != nil {
+		t.Fatalf("cmd.Run: %v", err)
+	}
+	return cmd
+}
+
 func TestIndexDeltaBasic(t *testing.T) {
 	type branchToDocumentMap map[string][]zoekt.Document