diff --git a/internal/devconfig/config.go b/internal/devconfig/config.go
index c7e38d02965..b029fd51fbd 100644
--- a/internal/devconfig/config.go
+++ b/internal/devconfig/config.go
@@ -141,8 +141,17 @@ func Find(path string) (*Config, error) {
 
 // searchDir looks for a config file in dir. It does not search parent
 // directories.
+//
+// In addition to a top-level devbox.json, searchDir also looks for the config
+// inside a .config subdirectory (.config/devbox.json). This lets users keep the
+// project root tidy by moving devbox's files out of the way, while still being
+// discoverable. A top-level devbox.json always takes precedence over one in
+// .config.
 func searchDir(dir string) (*Config, error) {
-	try := []string{configfile.DefaultName}
+	try := []string{
+		configfile.DefaultName,
+		filepath.Join(".config", configfile.DefaultName),
+	}
 	for _, name := range try {
 		path := filepath.Join(dir, name)
 		slog.Debug("trying config file", "path", path)
diff --git a/internal/devconfig/config_test.go b/internal/devconfig/config_test.go
index 9f747796156..c4f29521969 100644
--- a/internal/devconfig/config_test.go
+++ b/internal/devconfig/config_test.go
@@ -49,6 +49,69 @@ func TestOpen(t *testing.T) {
 	})
 }
 
+func TestOpenDotConfig(t *testing.T) {
+	t.Run("FindsConfigInDotConfigDir", func(t *testing.T) {
+		root, _, _ := mkNestedDirs(t)
+		dotConfig := filepath.Join(root, ".config")
+		if err := os.MkdirAll(dotConfig, 0o777); err != nil {
+			t.Fatalf("os.MkdirAll(%q) error: %v", dotConfig, err)
+		}
+		if _, err := Init(dotConfig); err != nil {
+			t.Fatalf("Init(%q) error: %v", dotConfig, err)
+		}
+
+		cfg, err := Open(root)
+		if err != nil {
+			t.Fatalf("Open(%q) error: %v", root, err)
+		}
+		want := filepath.Join(dotConfig, configfile.DefaultName)
+		if cfg.Root.AbsRootPath != want {
+			t.Errorf("cfg.Root.AbsRootPath = %q, want %q", cfg.Root.AbsRootPath, want)
+		}
+	})
+	t.Run("TopLevelConfigTakesPrecedence", func(t *testing.T) {
+		root, _, _ := mkNestedDirs(t)
+		dotConfig := filepath.Join(root, ".config")
+		if err := os.MkdirAll(dotConfig, 0o777); err != nil {
+			t.Fatalf("os.MkdirAll(%q) error: %v", dotConfig, err)
+		}
+		if _, err := Init(root); err != nil {
+			t.Fatalf("Init(%q) error: %v", root, err)
+		}
+		if _, err := Init(dotConfig); err != nil {
+			t.Fatalf("Init(%q) error: %v", dotConfig, err)
+		}
+
+		cfg, err := Open(root)
+		if err != nil {
+			t.Fatalf("Open(%q) error: %v", root, err)
+		}
+		want := filepath.Join(root, configfile.DefaultName)
+		if cfg.Root.AbsRootPath != want {
+			t.Errorf("cfg.Root.AbsRootPath = %q, want %q", cfg.Root.AbsRootPath, want)
+		}
+	})
+	t.Run("FindWalksUpToParentDotConfig", func(t *testing.T) {
+		root, child, _ := mkNestedDirs(t)
+		dotConfig := filepath.Join(root, ".config")
+		if err := os.MkdirAll(dotConfig, 0o777); err != nil {
+			t.Fatalf("os.MkdirAll(%q) error: %v", dotConfig, err)
+		}
+		if _, err := Init(dotConfig); err != nil {
+			t.Fatalf("Init(%q) error: %v", dotConfig, err)
+		}
+
+		cfg, err := Find(child)
+		if err != nil {
+			t.Fatalf("Find(%q) error: %v", child, err)
+		}
+		want := filepath.Join(dotConfig, configfile.DefaultName)
+		if cfg.Root.AbsRootPath != want {
+			t.Errorf("cfg.Root.AbsRootPath = %q, want %q", cfg.Root.AbsRootPath, want)
+		}
+	})
+}
+
 func TestOpenError(t *testing.T) {
 	t.Run("NotExist", func(t *testing.T) {
 		root, _, _ := mkNestedDirs(t)