diff --git a/agent/agentfiles/files.go b/agent/agentfiles/files.go
index 75c2c73c68..b526c60eba 100644
--- a/agent/agentfiles/files.go
+++ b/agent/agentfiles/files.go
@@ -333,22 +333,68 @@ func (api *API) writeFile(ctx context.Context, r *http.Request, path string) (HT
 		return status, err
 	}
 
-	f, err := api.filesystem.Create(path)
+	// Check if the target already exists so we can preserve its
+	// permissions on the temp file before rename.
+	var origMode os.FileMode
+	var haveOrigMode bool
+	if stat, serr := api.filesystem.Stat(path); serr == nil {
+		if stat.IsDir() {
+			return http.StatusBadRequest, xerrors.Errorf("open %s: is a directory", path)
+		}
+		origMode = stat.Mode()
+		haveOrigMode = true
+	}
+
+	// Write to a temp file in the same directory so the rename is
+	// always on the same device (atomic).
+	tmpfile, err := afero.TempFile(api.filesystem, dir, filepath.Base(path))
 	if err != nil {
 		status := http.StatusInternalServerError
-		switch {
-		case errors.Is(err, os.ErrPermission):
+		if errors.Is(err, os.ErrPermission) {
 			status = http.StatusForbidden
-		case errors.Is(err, syscall.EISDIR):
-			status = http.StatusBadRequest
 		}
 		return status, err
 	}
-	defer f.Close()
+	tmpName := tmpfile.Name()
 
-	_, err = io.Copy(f, r.Body)
-	if err != nil && !errors.Is(err, io.EOF) && ctx.Err() == nil {
-		api.logger.Error(ctx, "workspace agent write file", slog.Error(err))
+	_, err = io.Copy(tmpfile, r.Body)
+	if err != nil && !errors.Is(err, io.EOF) {
+		_ = tmpfile.Close()
+		if rerr := api.filesystem.Remove(tmpName); rerr != nil {
+			api.logger.Warn(ctx, "unable to clean up temp file", slog.Error(rerr))
+		}
+		return http.StatusInternalServerError, xerrors.Errorf("write %s: %w", path, err)
+	}
+
+	// Close before rename to flush buffered data and catch write
+	// errors (e.g. delayed allocation failures).
+	if err := tmpfile.Close(); err != nil {
+		if rerr := api.filesystem.Remove(tmpName); rerr != nil {
+			api.logger.Warn(ctx, "unable to clean up temp file", slog.Error(rerr))
+		}
+		return http.StatusInternalServerError, xerrors.Errorf("write %s: %w", path, err)
+	}
+
+	// Set permissions on the temp file before rename so there is
+	// no window where the target has wrong permissions.
+	if haveOrigMode {
+		if err := api.filesystem.Chmod(tmpName, origMode); err != nil {
+			api.logger.Warn(ctx, "unable to set file permissions",
+				slog.F("path", path),
+				slog.Error(err),
+			)
+		}
+	}
+
+	if err := api.filesystem.Rename(tmpName, path); err != nil {
+		if rerr := api.filesystem.Remove(tmpName); rerr != nil {
+			api.logger.Warn(ctx, "unable to clean up temp file", slog.Error(rerr))
+		}
+		status := http.StatusInternalServerError
+		if errors.Is(err, os.ErrPermission) {
+			status = http.StatusForbidden
+		}
+		return status, err
 	}
 
 	return 0, nil
@@ -460,18 +506,44 @@ func (api *API) editFile(ctx context.Context, path string, edits []workspacesdk.
 	if err != nil {
 		return http.StatusInternalServerError, err
 	}
-	defer tmpfile.Close()
+	tmpName := tmpfile.Name()
 
 	if _, err := tmpfile.Write([]byte(content)); err != nil {
-		if rerr := api.filesystem.Remove(tmpfile.Name()); rerr != nil {
+		_ = tmpfile.Close()
+		if rerr := api.filesystem.Remove(tmpName); rerr != nil {
 			api.logger.Warn(ctx, "unable to clean up temp file", slog.Error(rerr))
 		}
 		return http.StatusInternalServerError, xerrors.Errorf("edit %s: %w", path, err)
 	}
 
-	err = api.filesystem.Rename(tmpfile.Name(), path)
+	// Close before rename to flush buffered data and catch write
+	// errors (e.g. delayed allocation failures).
+	if err := tmpfile.Close(); err != nil {
+		if rerr := api.filesystem.Remove(tmpName); rerr != nil {
+			api.logger.Warn(ctx, "unable to clean up temp file", slog.Error(rerr))
+		}
+		return http.StatusInternalServerError, xerrors.Errorf("edit %s: %w", path, err)
+	}
+
+	// Set permissions on the temp file before rename so there is
+	// no window where the target has wrong permissions.
+	if err := api.filesystem.Chmod(tmpName, stat.Mode()); err != nil {
+		api.logger.Warn(ctx, "unable to set file permissions",
+			slog.F("path", path),
+			slog.Error(err),
+		)
+	}
+
+	err = api.filesystem.Rename(tmpName, path)
 	if err != nil {
-		return http.StatusInternalServerError, err
+		if rerr := api.filesystem.Remove(tmpName); rerr != nil {
+			api.logger.Warn(ctx, "unable to clean up temp file", slog.Error(rerr))
+		}
+		status := http.StatusInternalServerError
+		if errors.Is(err, os.ErrPermission) {
+			status = http.StatusForbidden
+		}
+		return status, err
 	}
 
 	return 0, nil
diff --git a/agent/agentfiles/files_test.go b/agent/agentfiles/files_test.go
index 6290de25e7..a59204429e 100644
--- a/agent/agentfiles/files_test.go
+++ b/agent/agentfiles/files_test.go
@@ -14,6 +14,7 @@ import (
 	"strings"
 	"syscall"
 	"testing"
+	"testing/iotest"
 
 	"github.com/go-chi/chi/v5"
 	"github.com/google/uuid"
@@ -399,6 +400,83 @@ func TestWriteFile(t *testing.T) {
 	}
 }
 
+func TestWriteFile_ReportsIOError(t *testing.T) {
+	t.Parallel()
+
+	logger := slogtest.Make(t, &slogtest.Options{IgnoreErrors: true}).Leveled(slog.LevelDebug)
+	fs := afero.NewMemMapFs()
+	api := agentfiles.NewAPI(logger, fs, nil)
+
+	tmpdir := os.TempDir()
+	path := filepath.Join(tmpdir, "write-io-error")
+	err := afero.WriteFile(fs, path, []byte("original"), 0o644)
+	require.NoError(t, err)
+
+	ctx, cancel := context.WithTimeout(context.Background(), testutil.WaitShort)
+	defer cancel()
+
+	// A reader that always errors simulates a failed body read
+	// (e.g. network interruption). The atomic write should leave
+	// the original file intact.
+	body := iotest.ErrReader(xerrors.New("simulated I/O error"))
+	w := httptest.NewRecorder()
+	r := httptest.NewRequestWithContext(ctx, http.MethodPost,
+		fmt.Sprintf("/write-file?path=%s", path), body)
+	api.Routes().ServeHTTP(w, r)
+
+	require.Equal(t, http.StatusInternalServerError, w.Code)
+	got := &codersdk.Error{}
+	err = json.NewDecoder(w.Body).Decode(got)
+	require.NoError(t, err)
+	require.ErrorContains(t, got, "simulated I/O error")
+
+	// The original file must survive the failed write.
+	data, err := afero.ReadFile(fs, path)
+	require.NoError(t, err)
+	require.Equal(t, "original", string(data))
+}
+
+func TestWriteFile_PreservesPermissions(t *testing.T) {
+	t.Parallel()
+
+	if runtime.GOOS == "windows" {
+		t.Skip("file permissions are not reliably supported on Windows")
+	}
+
+	dir := t.TempDir()
+	logger := slogtest.Make(t, nil).Leveled(slog.LevelDebug)
+	osFs := afero.NewOsFs()
+	api := agentfiles.NewAPI(logger, osFs, nil)
+
+	path := filepath.Join(dir, "script.sh")
+	err := afero.WriteFile(osFs, path, []byte("#!/bin/sh\necho hello\n"), 0o755)
+	require.NoError(t, err)
+
+	info, err := osFs.Stat(path)
+	require.NoError(t, err)
+	require.Equal(t, os.FileMode(0o755), info.Mode().Perm())
+
+	ctx, cancel := context.WithTimeout(context.Background(), testutil.WaitShort)
+	defer cancel()
+
+	// Overwrite the file with new content.
+	w := httptest.NewRecorder()
+	r := httptest.NewRequestWithContext(ctx, http.MethodPost,
+		fmt.Sprintf("/write-file?path=%s", path),
+		bytes.NewReader([]byte("#!/bin/sh\necho world\n")))
+	api.Routes().ServeHTTP(w, r)
+	require.Equal(t, http.StatusOK, w.Code)
+
+	data, err := afero.ReadFile(osFs, path)
+	require.NoError(t, err)
+	require.Equal(t, "#!/bin/sh\necho world\n", string(data))
+
+	info, err = osFs.Stat(path)
+	require.NoError(t, err)
+	require.Equal(t, os.FileMode(0o755), info.Mode().Perm(),
+		"write_file should preserve the original file's permissions")
+}
+
 func TestEditFiles(t *testing.T) {
 	t.Parallel()
 
@@ -907,6 +985,67 @@ func TestEditFiles(t *testing.T) {
 	}
 }
 
+func TestEditFiles_PreservesPermissions(t *testing.T) {
+	t.Parallel()
+
+	if runtime.GOOS == "windows" {
+		t.Skip("file permissions are not reliably supported on Windows")
+	}
+
+	dir := t.TempDir()
+	logger := slogtest.Make(t, nil).Leveled(slog.LevelDebug)
+	osFs := afero.NewOsFs()
+	api := agentfiles.NewAPI(logger, osFs, nil)
+
+	path := filepath.Join(dir, "script.sh")
+	err := afero.WriteFile(osFs, path, []byte("#!/bin/sh\necho hello\n"), 0o755)
+	require.NoError(t, err)
+
+	// Sanity-check the initial mode.
+	info, err := osFs.Stat(path)
+	require.NoError(t, err)
+	require.Equal(t, os.FileMode(0o755), info.Mode().Perm())
+
+	ctx, cancel := context.WithTimeout(context.Background(), testutil.WaitShort)
+	defer cancel()
+
+	body := workspacesdk.FileEditRequest{
+		Files: []workspacesdk.FileEdits{
+			{
+				Path: path,
+				Edits: []workspacesdk.FileEdit{
+					{
+						Search:  "hello",
+						Replace: "world",
+					},
+				},
+			},
+		},
+	}
+	buf := bytes.NewBuffer(nil)
+	enc := json.NewEncoder(buf)
+	enc.SetEscapeHTML(false)
+	err = enc.Encode(body)
+	require.NoError(t, err)
+
+	w := httptest.NewRecorder()
+	r := httptest.NewRequestWithContext(ctx, http.MethodPost, "/edit-files", buf)
+	api.Routes().ServeHTTP(w, r)
+	require.Equal(t, http.StatusOK, w.Code)
+
+	// Verify content was updated.
+	data, err := afero.ReadFile(osFs, path)
+	require.NoError(t, err)
+	require.Equal(t, "#!/bin/sh\necho world\n", string(data))
+
+	// Verify permissions are preserved after the
+	// temp-file-and-rename cycle.
+	info, err = osFs.Stat(path)
+	require.NoError(t, err)
+	require.Equal(t, os.FileMode(0o755), info.Mode().Perm(),
+		"edit_files should preserve the original file's permissions")
+}
+
 func TestHandleWriteFile_ChatHeaders_UpdatesPathStore(t *testing.T) {
 	t.Parallel()