diff --git a/agent/api.go b/agent/api.go
index a3241feb3b7ee..259866797a3c4 100644
--- a/agent/api.go
+++ b/agent/api.go
@@ -41,6 +41,7 @@ func (a *agent) apiHandler() http.Handler {
 	r.Get("/api/v0/containers", ch.ServeHTTP)
 	r.Get("/api/v0/listening-ports", lp.handler)
 	r.Get("/api/v0/netcheck", a.HandleNetcheck)
+	r.Post("/api/v0/list-directory", a.HandleLS)
 	r.Get("/debug/logs", a.HandleHTTPDebugLogs)
 	r.Get("/debug/magicsock", a.HandleHTTPDebugMagicsock)
 	r.Get("/debug/magicsock/debug-logging/{state}", a.HandleHTTPMagicsockDebugLoggingState)
diff --git a/agent/ls.go b/agent/ls.go
new file mode 100644
index 0000000000000..1d8adea12e0b4
--- /dev/null
+++ b/agent/ls.go
@@ -0,0 +1,181 @@
+package agent
+
+import (
+	"errors"
+	"net/http"
+	"os"
+	"path/filepath"
+	"regexp"
+	"runtime"
+	"strings"
+
+	"github.com/shirou/gopsutil/v4/disk"
+	"golang.org/x/xerrors"
+
+	"github.com/coder/coder/v2/coderd/httpapi"
+	"github.com/coder/coder/v2/codersdk"
+)
+
+var WindowsDriveRegex = regexp.MustCompile(`^[a-zA-Z]:\\$`)
+
+func (*agent) HandleLS(rw http.ResponseWriter, r *http.Request) {
+	ctx := r.Context()
+
+	var query LSRequest
+	if !httpapi.Read(ctx, rw, r, &query) {
+		return
+	}
+
+	resp, err := listFiles(query)
+	if err != nil {
+		status := http.StatusInternalServerError
+		switch {
+		case errors.Is(err, os.ErrNotExist):
+			status = http.StatusNotFound
+		case errors.Is(err, os.ErrPermission):
+			status = http.StatusForbidden
+		default:
+		}
+		httpapi.Write(ctx, rw, status, codersdk.Response{
+			Message: err.Error(),
+		})
+		return
+	}
+
+	httpapi.Write(ctx, rw, http.StatusOK, resp)
+}
+
+func listFiles(query LSRequest) (LSResponse, error) {
+	var fullPath []string
+	switch query.Relativity {
+	case LSRelativityHome:
+		home, err := os.UserHomeDir()
+		if err != nil {
+			return LSResponse{}, xerrors.Errorf("failed to get user home directory: %w", err)
+		}
+		fullPath = []string{home}
+	case LSRelativityRoot:
+		if runtime.GOOS == "windows" {
+			if len(query.Path) == 0 {
+				return listDrives()
+			}
+			if !WindowsDriveRegex.MatchString(query.Path[0]) {
+				return LSResponse{}, xerrors.Errorf("invalid drive letter %q", query.Path[0])
+			}
+		} else {
+			fullPath = []string{"/"}
+		}
+	default:
+		return LSResponse{}, xerrors.Errorf("unsupported relativity type %q", query.Relativity)
+	}
+
+	fullPath = append(fullPath, query.Path...)
+	fullPathRelative := filepath.Join(fullPath...)
+	absolutePathString, err := filepath.Abs(fullPathRelative)
+	if err != nil {
+		return LSResponse{}, xerrors.Errorf("failed to get absolute path of %q: %w", fullPathRelative, err)
+	}
+
+	f, err := os.Open(absolutePathString)
+	if err != nil {
+		return LSResponse{}, xerrors.Errorf("failed to open directory %q: %w", absolutePathString, err)
+	}
+	defer f.Close()
+
+	stat, err := f.Stat()
+	if err != nil {
+		return LSResponse{}, xerrors.Errorf("failed to stat directory %q: %w", absolutePathString, err)
+	}
+
+	if !stat.IsDir() {
+		return LSResponse{}, xerrors.Errorf("path %q is not a directory", absolutePathString)
+	}
+
+	// `contents` may be partially populated even if the operation fails midway.
+	contents, _ := f.ReadDir(-1)
+	respContents := make([]LSFile, 0, len(contents))
+	for _, file := range contents {
+		respContents = append(respContents, LSFile{
+			Name:               file.Name(),
+			AbsolutePathString: filepath.Join(absolutePathString, file.Name()),
+			IsDir:              file.IsDir(),
+		})
+	}
+
+	absolutePath := pathToArray(absolutePathString)
+
+	return LSResponse{
+		AbsolutePath:       absolutePath,
+		AbsolutePathString: absolutePathString,
+		Contents:           respContents,
+	}, nil
+}
+
+func listDrives() (LSResponse, error) {
+	partitionStats, err := disk.Partitions(true)
+	if err != nil {
+		return LSResponse{}, xerrors.Errorf("failed to get partitions: %w", err)
+	}
+	contents := make([]LSFile, 0, len(partitionStats))
+	for _, a := range partitionStats {
+		// Drive letters on Windows have a trailing separator as part of their name.
+		// i.e. `os.Open("C:")` does not work, but `os.Open("C:\\")` does.
+		name := a.Mountpoint + string(os.PathSeparator)
+		contents = append(contents, LSFile{
+			Name:               name,
+			AbsolutePathString: name,
+			IsDir:              true,
+		})
+	}
+
+	return LSResponse{
+		AbsolutePath:       []string{},
+		AbsolutePathString: "",
+		Contents:           contents,
+	}, nil
+}
+
+func pathToArray(path string) []string {
+	out := strings.FieldsFunc(path, func(r rune) bool {
+		return r == os.PathSeparator
+	})
+	// Drive letters on Windows have a trailing separator as part of their name.
+	// i.e. `os.Open("C:")` does not work, but `os.Open("C:\\")` does.
+	if runtime.GOOS == "windows" && len(out) > 0 {
+		out[0] += string(os.PathSeparator)
+	}
+	return out
+}
+
+type LSRequest struct {
+	// e.g. [], ["repos", "coder"],
+	Path []string `json:"path"`
+	// Whether the supplied path is relative to the user's home directory,
+	// or the root directory.
+	Relativity LSRelativity `json:"relativity"`
+}
+
+type LSResponse struct {
+	AbsolutePath []string `json:"absolute_path"`
+	// Returned so clients can display the full path to the user, and
+	// copy it to configure file sync
+	// e.g. Windows: "C:\\Users\\coder"
+	//      Linux: "/home/coder"
+	AbsolutePathString string   `json:"absolute_path_string"`
+	Contents           []LSFile `json:"contents"`
+}
+
+type LSFile struct {
+	Name string `json:"name"`
+	// e.g. "C:\\Users\\coder\\hello.txt"
+	//      "/home/coder/hello.txt"
+	AbsolutePathString string `json:"absolute_path_string"`
+	IsDir              bool   `json:"is_dir"`
+}
+
+type LSRelativity string
+
+const (
+	LSRelativityRoot LSRelativity = "root"
+	LSRelativityHome LSRelativity = "home"
+)
diff --git a/agent/ls_internal_test.go b/agent/ls_internal_test.go
new file mode 100644
index 0000000000000..acc4ea2929444
--- /dev/null
+++ b/agent/ls_internal_test.go
@@ -0,0 +1,207 @@
+package agent
+
+import (
+	"os"
+	"path/filepath"
+	"runtime"
+	"testing"
+
+	"github.com/stretchr/testify/require"
+)
+
+func TestListFilesNonExistentDirectory(t *testing.T) {
+	t.Parallel()
+
+	query := LSRequest{
+		Path:       []string{"idontexist"},
+		Relativity: LSRelativityHome,
+	}
+	_, err := listFiles(query)
+	require.ErrorIs(t, err, os.ErrNotExist)
+}
+
+func TestListFilesPermissionDenied(t *testing.T) {
+	t.Parallel()
+
+	if runtime.GOOS == "windows" {
+		t.Skip("creating an unreadable-by-user directory is non-trivial on Windows")
+	}
+
+	home, err := os.UserHomeDir()
+	require.NoError(t, err)
+
+	tmpDir := t.TempDir()
+
+	reposDir := filepath.Join(tmpDir, "repos")
+	err = os.Mkdir(reposDir, 0o000)
+	require.NoError(t, err)
+
+	rel, err := filepath.Rel(home, reposDir)
+	require.NoError(t, err)
+
+	query := LSRequest{
+		Path:       pathToArray(rel),
+		Relativity: LSRelativityHome,
+	}
+	_, err = listFiles(query)
+	require.ErrorIs(t, err, os.ErrPermission)
+}
+
+func TestListFilesNotADirectory(t *testing.T) {
+	t.Parallel()
+
+	home, err := os.UserHomeDir()
+	require.NoError(t, err)
+
+	tmpDir := t.TempDir()
+
+	filePath := filepath.Join(tmpDir, "file.txt")
+	err = os.WriteFile(filePath, []byte("content"), 0o600)
+	require.NoError(t, err)
+
+	rel, err := filepath.Rel(home, filePath)
+	require.NoError(t, err)
+
+	query := LSRequest{
+		Path:       pathToArray(rel),
+		Relativity: LSRelativityHome,
+	}
+	_, err = listFiles(query)
+	require.ErrorContains(t, err, "is not a directory")
+}
+
+func TestListFilesSuccess(t *testing.T) {
+	t.Parallel()
+
+	tc := []struct {
+		name       string
+		baseFunc   func(t *testing.T) string
+		relativity LSRelativity
+	}{
+		{
+			name: "home",
+			baseFunc: func(t *testing.T) string {
+				home, err := os.UserHomeDir()
+				require.NoError(t, err)
+				return home
+			},
+			relativity: LSRelativityHome,
+		},
+		{
+			name: "root",
+			baseFunc: func(*testing.T) string {
+				if runtime.GOOS == "windows" {
+					return ""
+				}
+				return "/"
+			},
+			relativity: LSRelativityRoot,
+		},
+	}
+
+	// nolint:paralleltest // Not since Go v1.22.
+	for _, tc := range tc {
+		t.Run(tc.name, func(t *testing.T) {
+			t.Parallel()
+
+			base := tc.baseFunc(t)
+			tmpDir := t.TempDir()
+
+			reposDir := filepath.Join(tmpDir, "repos")
+			err := os.Mkdir(reposDir, 0o755)
+			require.NoError(t, err)
+
+			downloadsDir := filepath.Join(tmpDir, "Downloads")
+			err = os.Mkdir(downloadsDir, 0o755)
+			require.NoError(t, err)
+
+			textFile := filepath.Join(tmpDir, "file.txt")
+			err = os.WriteFile(textFile, []byte("content"), 0o600)
+			require.NoError(t, err)
+
+			var queryComponents []string
+			// We can't get an absolute path relative to empty string on Windows.
+			if runtime.GOOS == "windows" && base == "" {
+				queryComponents = pathToArray(tmpDir)
+			} else {
+				rel, err := filepath.Rel(base, tmpDir)
+				require.NoError(t, err)
+				queryComponents = pathToArray(rel)
+			}
+
+			query := LSRequest{
+				Path:       queryComponents,
+				Relativity: tc.relativity,
+			}
+			resp, err := listFiles(query)
+			require.NoError(t, err)
+
+			require.Equal(t, tmpDir, resp.AbsolutePathString)
+			require.ElementsMatch(t, []LSFile{
+				{
+					Name:               "repos",
+					AbsolutePathString: reposDir,
+					IsDir:              true,
+				},
+				{
+					Name:               "Downloads",
+					AbsolutePathString: downloadsDir,
+					IsDir:              true,
+				},
+				{
+					Name:               "file.txt",
+					AbsolutePathString: textFile,
+					IsDir:              false,
+				},
+			}, resp.Contents)
+		})
+	}
+}
+
+func TestListFilesListDrives(t *testing.T) {
+	t.Parallel()
+
+	if runtime.GOOS != "windows" {
+		t.Skip("skipping test on non-Windows OS")
+	}
+
+	query := LSRequest{
+		Path:       []string{},
+		Relativity: LSRelativityRoot,
+	}
+	resp, err := listFiles(query)
+	require.NoError(t, err)
+	require.Contains(t, resp.Contents, LSFile{
+		Name:               "C:\\",
+		AbsolutePathString: "C:\\",
+		IsDir:              true,
+	})
+
+	query = LSRequest{
+		Path:       []string{"C:\\"},
+		Relativity: LSRelativityRoot,
+	}
+	resp, err = listFiles(query)
+	require.NoError(t, err)
+
+	query = LSRequest{
+		Path:       resp.AbsolutePath,
+		Relativity: LSRelativityRoot,
+	}
+	resp, err = listFiles(query)
+	require.NoError(t, err)
+	// System directory should always exist
+	require.Contains(t, resp.Contents, LSFile{
+		Name:               "Windows",
+		AbsolutePathString: "C:\\Windows",
+		IsDir:              true,
+	})
+
+	query = LSRequest{
+		// Network drives are not supported.
+		Path:       []string{"\\sshfs\\work"},
+		Relativity: LSRelativityRoot,
+	}
+	resp, err = listFiles(query)
+	require.ErrorContains(t, err, "drive")
+}
diff --git a/go.mod b/go.mod
index 4b38c65265f4d..1e68a84f47002 100644
--- a/go.mod
+++ b/go.mod
@@ -164,6 +164,7 @@ require (
 	github.com/prometheus/common v0.62.0
 	github.com/quasilyte/go-ruleguard/dsl v0.3.21
 	github.com/robfig/cron/v3 v3.0.1
+	github.com/shirou/gopsutil/v4 v4.25.2
 	github.com/skratchdot/open-golang v0.0.0-20200116055534-eef842397966
 	github.com/spf13/afero v1.12.0
 	github.com/spf13/pflag v1.0.5
@@ -285,7 +286,7 @@ require (
 	github.com/dop251/goja v0.0.0-20241024094426-79f3a7efcdbd // indirect
 	github.com/dustin/go-humanize v1.0.1
 	github.com/eapache/queue/v2 v2.0.0-20230407133247-75960ed334e4 // indirect
-	github.com/ebitengine/purego v0.6.0-alpha.5 // indirect
+	github.com/ebitengine/purego v0.8.2 // indirect
 	github.com/elastic/go-windows v1.0.0 // indirect
 	github.com/erikgeiser/coninput v0.0.0-20211004153227-1c3628e74d0f // indirect
 	github.com/felixge/httpsnoop v1.0.4 // indirect
diff --git a/go.sum b/go.sum
index 6496dfc84118d..bd29a7b7bef56 100644
--- a/go.sum
+++ b/go.sum
@@ -301,8 +301,8 @@ github.com/dustin/go-humanize v1.0.1 h1:GzkhY7T5VNhEkwH0PVJgjz+fX1rhBrR7pRT3mDkp
 github.com/dustin/go-humanize v1.0.1/go.mod h1:Mu1zIs6XwVuF/gI1OepvI0qD18qycQx+mFykh5fBlto=
 github.com/eapache/queue/v2 v2.0.0-20230407133247-75960ed334e4 h1:8EXxF+tCLqaVk8AOC29zl2mnhQjwyLxxOTuhUazWRsg=
 github.com/eapache/queue/v2 v2.0.0-20230407133247-75960ed334e4/go.mod h1:I5sHm0Y0T1u5YjlyqC5GVArM7aNZRUYtTjmJ8mPJFds=
-github.com/ebitengine/purego v0.6.0-alpha.5 h1:EYID3JOAdmQ4SNZYJHu9V6IqOeRQDBYxqKAg9PyoHFY=
-github.com/ebitengine/purego v0.6.0-alpha.5/go.mod h1:ah1In8AOtksoNK6yk5z1HTJeUkC1Ez4Wk2idgGslMwQ=
+github.com/ebitengine/purego v0.8.2 h1:jPPGWs2sZ1UgOSgD2bClL0MJIqu58nOmIcBuXr62z1I=
+github.com/ebitengine/purego v0.8.2/go.mod h1:iIjxzd6CiRiOG0UyXP+V1+jWqUXVjPKLAI0mRfJZTmQ=
 github.com/elastic/go-sysinfo v1.15.0 h1:54pRFlAYUlVNQ2HbXzLVZlV+fxS7Eax49stzg95M4Xw=
 github.com/elastic/go-sysinfo v1.15.0/go.mod h1:jPSuTgXG+dhhh0GKIyI2Cso+w5lPJ5PvVqKlL8LV/Hk=
 github.com/elastic/go-windows v1.0.0 h1:qLURgZFkkrYyTTkvYpsZIgf83AUsdIHfvlJaqaZ7aSY=
@@ -825,6 +825,8 @@ github.com/sergi/go-diff v1.3.2-0.20230802210424-5b0b94c5c0d3 h1:n661drycOFuPLCN
 github.com/sergi/go-diff v1.3.2-0.20230802210424-5b0b94c5c0d3/go.mod h1:A0bzQcvG0E7Rwjx0REVgAGH58e96+X0MeOfepqsbeW4=
 github.com/shirou/gopsutil/v3 v3.24.4 h1:dEHgzZXt4LMNm+oYELpzl9YCqV65Yr/6SfrvgRBtXeU=
 github.com/shirou/gopsutil/v3 v3.24.4/go.mod h1:lTd2mdiOspcqLgAnr9/nGi71NkeMpWKdmhuxm9GusH8=
+github.com/shirou/gopsutil/v4 v4.25.2 h1:NMscG3l2CqtWFS86kj3vP7soOczqrQYIEhO/pMvvQkk=
+github.com/shirou/gopsutil/v4 v4.25.2/go.mod h1:34gBYJzyqCDT11b6bMHP0XCvWeU3J61XRT7a2EmCRTA=
 github.com/shoenig/go-m1cpu v0.1.6 h1:nxdKQNcEB6vzgA2E2bvzKIYRuNj7XNJ4S/aRSwKzFtM=
 github.com/shoenig/go-m1cpu v0.1.6/go.mod h1:1JJMcUBvfNwpq05QDQVAnx3gUHr9IYF7GNg9SUEw2VQ=
 github.com/shoenig/test v0.6.4 h1:kVTaSd7WLz5WZ2IaoM0RSzRsUD+m8wRR+5qvntpn4LU=