diff --git a/internal/boxcli/init.go b/internal/boxcli/init.go
index 31ba559564f..1e14616c38d 100644
--- a/internal/boxcli/init.go
+++ b/internal/boxcli/init.go
@@ -36,7 +36,7 @@ func initCmd() *cobra.Command {
 				path, _ = os.Getwd()
 			}
 			if errors.Is(err, os.ErrExist) {
-				ux.Fwarningf(cmd.ErrOrStderr(), "devbox.json already exists in %q.", path)
+				ux.Fwarningf(cmd.ErrOrStderr(), "A devbox config already exists in %q.", path)
 				return nil
 			}
 			if err != nil {
diff --git a/internal/boxcli/multi/multi.go b/internal/boxcli/multi/multi.go
index 0a2cae34cdf..a98d28ef060 100644
--- a/internal/boxcli/multi/multi.go
+++ b/internal/boxcli/multi/multi.go
@@ -3,6 +3,7 @@ package multi
 import (
 	"io/fs"
 	"path/filepath"
+	"slices"
 
 	"go.jetify.com/devbox/internal/debug"
 	"go.jetify.com/devbox/internal/devbox"
@@ -14,6 +15,10 @@ func Open(opts *devopt.Opts) ([]*devbox.Devbox, error) {
 	defer debug.FunctionTimer().End()
 
 	var boxes []*devbox.Devbox
+	// A single directory may contain more than one recognized config name
+	// (e.g. both devbox.json and devbox.jsonc). Track the directories already
+	// opened so each project is opened exactly once.
+	seenDirs := map[string]bool{}
 	err := filepath.WalkDir(
 		".",
 		func(path string, dirEntry fs.DirEntry, err error) error {
@@ -21,9 +26,17 @@ func Open(opts *devopt.Opts) ([]*devbox.Devbox, error) {
 				return err
 			}
 
-			if !dirEntry.IsDir() && filepath.Base(path) == configfile.DefaultName {
+			if !dirEntry.IsDir() && slices.Contains(configfile.ValidNames, filepath.Base(path)) {
+				dir := filepath.Dir(path)
+				if seenDirs[dir] {
+					return nil
+				}
+				seenDirs[dir] = true
+
 				optsCopy := *opts
-				optsCopy.Dir = path
+				// Open by directory so devconfig applies its filename
+				// precedence (devbox.json wins over devbox.jsonc).
+				optsCopy.Dir = dir
 				box, err := devbox.Open(&optsCopy)
 				if err != nil {
 					return err
diff --git a/internal/boxcli/multi/multi_test.go b/internal/boxcli/multi/multi_test.go
new file mode 100644
index 00000000000..1ee18d52088
--- /dev/null
+++ b/internal/boxcli/multi/multi_test.go
@@ -0,0 +1,44 @@
+package multi
+
+import (
+	"io"
+	"os"
+	"path/filepath"
+	"testing"
+
+	"go.jetify.com/devbox/internal/devbox/devopt"
+	"go.jetify.com/devbox/internal/devconfig/configfile"
+)
+
+// TestOpenDeduplicatesConfigsInSameDir ensures that a directory containing more
+// than one recognized config name (e.g. both devbox.json and devbox.jsonc) is
+// opened only once, so `--all-projects` commands don't run twice for it.
+func TestOpenDeduplicatesConfigsInSameDir(t *testing.T) {
+	root := t.TempDir()
+
+	// projBoth has both config names; projJSON has only devbox.json.
+	projBoth := filepath.Join(root, "projBoth")
+	projJSON := filepath.Join(root, "projJSON")
+	for _, dir := range []string{projBoth, projJSON} {
+		if err := os.MkdirAll(dir, 0o755); err != nil {
+			t.Fatal(err)
+		}
+		if err := os.WriteFile(filepath.Join(dir, configfile.DefaultName), []byte(`{"packages": []}`), 0o644); err != nil {
+			t.Fatal(err)
+		}
+	}
+	if err := os.WriteFile(filepath.Join(projBoth, configfile.AltName), []byte(`{"packages": []}`), 0o644); err != nil {
+		t.Fatal(err)
+	}
+
+	// multi.Open walks the current working directory.
+	t.Chdir(root)
+
+	boxes, err := Open(&devopt.Opts{Stderr: io.Discard})
+	if err != nil {
+		t.Fatalf("Open() error: %v", err)
+	}
+	if len(boxes) != 2 {
+		t.Errorf("Open() opened %d projects, want 2 (projBoth must be opened once despite having both config names)", len(boxes))
+	}
+}
diff --git a/internal/devbox/devbox.go b/internal/devbox/devbox.go
index c26b3257a65..50d49424123 100644
--- a/internal/devbox/devbox.go
+++ b/internal/devbox/devbox.go
@@ -502,6 +502,7 @@ func (d *Devbox) GenerateDevcontainer(ctx context.Context, generateOpts devopt.G
 		IsDevcontainer: true,
 		Pkgs:           d.AllPackageNamesIncludingRemovedTriggerPackages(),
 		LocalFlakeDirs: d.getLocalFlakesDirs(),
+		ConfigFileName: d.cfg.Root.FileName(),
 	}
 
 	// generate dockerfile
@@ -541,6 +542,7 @@ func (d *Devbox) GenerateDockerfile(ctx context.Context, generateOpts devopt.Gen
 		IsDevcontainer: false,
 		Pkgs:           d.AllPackageNamesIncludingRemovedTriggerPackages(),
 		LocalFlakeDirs: d.getLocalFlakesDirs(),
+		ConfigFileName: d.cfg.Root.FileName(),
 	}
 
 	scripts := d.cfg.Scripts()
diff --git a/internal/devbox/generate/devcontainer_util.go b/internal/devbox/generate/devcontainer_util.go
index 9cbe36c1cbd..34b3317010c 100644
--- a/internal/devbox/generate/devcontainer_util.go
+++ b/internal/devbox/generate/devcontainer_util.go
@@ -23,6 +23,7 @@ import (
 	"github.com/samber/lo"
 	"go.jetify.com/devbox/internal/boxcli/usererr"
 	"go.jetify.com/devbox/internal/devbox/devopt"
+	"go.jetify.com/devbox/internal/devconfig/configfile"
 )
 
 //go:embed tmpl/*
@@ -34,6 +35,10 @@ type Options struct {
 	IsDevcontainer bool
 	Pkgs           []string
 	LocalFlakeDirs []string
+	// ConfigFileName is the basename of the project's config file
+	// (devbox.json or devbox.jsonc) so generated Dockerfiles copy the right
+	// one. Defaults to devbox.json when empty.
+	ConfigFileName string
 }
 
 type devcontainerObject struct {
@@ -112,6 +117,7 @@ func (g *Options) CreateDockerfile(
 		"IsDevcontainer": g.IsDevcontainer,
 		"RootUser":       g.RootUser,
 		"LocalFlakeDirs": g.LocalFlakeDirs,
+		"ConfigFileName": cmp.Or(g.ConfigFileName, configfile.DefaultName),
 
 		// The following are only used for prod Dockerfile
 		"DevboxRunInstall": lo.Ternary(opts.HasInstall, "devbox run install", "echo 'No install script found, skipping'"),
diff --git a/internal/devbox/generate/devcontainer_util_test.go b/internal/devbox/generate/devcontainer_util_test.go
index f74edf88673..df81ecd7a9b 100644
--- a/internal/devbox/generate/devcontainer_util_test.go
+++ b/internal/devbox/generate/devcontainer_util_test.go
@@ -54,3 +54,32 @@ func generateDevDockerfile(t *testing.T, rootUser bool) string {
 	}
 	return string(contents)
 }
+
+// TestCreateDockerfileDevCopiesConfigFileName ensures the generated dev
+// Dockerfile copies the project's actual config file, which may be named
+// devbox.jsonc rather than devbox.json.
+func TestCreateDockerfileDevCopiesConfigFileName(t *testing.T) {
+	for _, name := range []string{"", "devbox.json", "devbox.jsonc"} {
+		dir := t.TempDir()
+		g := &Options{Path: dir, ConfigFileName: name}
+		if err := g.CreateDockerfile(t.Context(), CreateDockerfileOptions{ForType: "dev"}); err != nil {
+			t.Fatalf("CreateDockerfile(ConfigFileName=%q) failed: %v", name, err)
+		}
+		contents, err := os.ReadFile(filepath.Join(dir, "Dockerfile"))
+		if err != nil {
+			t.Fatal(err)
+		}
+		want := name
+		if want == "" {
+			want = "devbox.json"
+		}
+		// Non-root images use `COPY --chown=... <src> <dst>`; match on the
+		// trailing "<src> <dst>" pair so both forms are covered.
+		if !strings.Contains(string(contents), " "+want+" "+want+"\n") {
+			t.Errorf("ConfigFileName=%q: Dockerfile should copy %s, got:\n%s", name, want, contents)
+		}
+		if want != "devbox.json" && strings.Contains(string(contents), " devbox.json devbox.json") {
+			t.Errorf("ConfigFileName=%q: Dockerfile should not also copy devbox.json, got:\n%s", name, contents)
+		}
+	}
+}
diff --git a/internal/devbox/generate/tmpl/dev.Dockerfile.tmpl b/internal/devbox/generate/tmpl/dev.Dockerfile.tmpl
index 325b238e7f8..259d5fd0019 100644
--- a/internal/devbox/generate/tmpl/dev.Dockerfile.tmpl
+++ b/internal/devbox/generate/tmpl/dev.Dockerfile.tmpl
@@ -8,10 +8,10 @@ WORKDIR /code
 USER root:root
 RUN mkdir -p /code && chown ${DEVBOX_USER}:${DEVBOX_USER} /code
 USER ${DEVBOX_USER}:${DEVBOX_USER}
-COPY --chown=${DEVBOX_USER}:${DEVBOX_USER} devbox.json devbox.json
+COPY --chown=${DEVBOX_USER}:${DEVBOX_USER} {{.ConfigFileName}} {{.ConfigFileName}}
 COPY --chown=${DEVBOX_USER}:${DEVBOX_USER} devbox.lock devbox.lock
 {{- else}}
-COPY devbox.json devbox.json
+COPY {{.ConfigFileName}} {{.ConfigFileName}}
 COPY devbox.lock devbox.lock
 {{- end}}
 
diff --git a/internal/devbox/generate/tmpl/envrcContent.tmpl b/internal/devbox/generate/tmpl/envrcContent.tmpl
index b68bbbc7204..5b02f675799 100644
--- a/internal/devbox/generate/tmpl/envrcContent.tmpl
+++ b/internal/devbox/generate/tmpl/envrcContent.tmpl
@@ -1,6 +1,6 @@
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias{{ if .EnvFlag }} {{ .EnvFlag }}{{ end }}{{ if .ConfigDir }} {{ .ConfigDir }}{{ end }})"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 {{ if .EnvFile }}
diff --git a/internal/devconfig/config.go b/internal/devconfig/config.go
index fd249780471..c60b1b8cd00 100644
--- a/internal/devconfig/config.go
+++ b/internal/devconfig/config.go
@@ -142,8 +142,7 @@ func Find(path string) (*Config, error) {
 // searchDir looks for a config file in dir. It does not search parent
 // directories.
 func searchDir(dir string) (*Config, error) {
-	try := []string{configfile.DefaultName}
-	for _, name := range try {
+	for _, name := range configfile.ValidNames {
 		path := filepath.Join(dir, name)
 		slog.Debug("trying config file", "path", path)
 
@@ -156,7 +155,7 @@ func searchDir(dir string) (*Config, error) {
 		if errors.Is(err, os.ErrNotExist) {
 			continue
 		}
-		// Ignore directories named devbox.json.
+		// Ignore directories that happen to share a config filename.
 		if errors.Is(err, errIsDirectory) {
 			continue
 		}
diff --git a/internal/devconfig/config_test.go b/internal/devconfig/config_test.go
index 7303fbb8163..d7d8924d8ab 100644
--- a/internal/devconfig/config_test.go
+++ b/internal/devconfig/config_test.go
@@ -282,6 +282,86 @@ func TestFindError(t *testing.T) {
 	})
 }
 
+func TestJSONCConfig(t *testing.T) {
+	const jsonc = "{\n  // devbox lets you comment your config\n  \"packages\": []\n}\n"
+
+	t.Run("OpenDiscoversJSONC", func(t *testing.T) {
+		dir := t.TempDir()
+		path := filepath.Join(dir, configfile.AltName)
+		if err := os.WriteFile(path, []byte(jsonc), 0o644); err != nil {
+			t.Fatal(err)
+		}
+
+		cfg, err := Open(dir)
+		if err != nil {
+			t.Fatalf("Open(%q) error: %v", dir, err)
+		}
+		if cfg.Root.AbsRootPath != path {
+			t.Errorf("cfg.Root.AbsRootPath = %q, want %q", cfg.Root.AbsRootPath, path)
+		}
+	})
+
+	t.Run("FindDiscoversJSONCInParent", func(t *testing.T) {
+		root, child, _ := mkNestedDirs(t)
+		path := filepath.Join(root, configfile.AltName)
+		if err := os.WriteFile(path, []byte(jsonc), 0o644); err != nil {
+			t.Fatal(err)
+		}
+
+		cfg, err := Find(child)
+		if err != nil {
+			t.Fatalf("Find(%q) error: %v", child, err)
+		}
+		if cfg.Root.AbsRootPath != path {
+			t.Errorf("cfg.Root.AbsRootPath = %q, want %q", cfg.Root.AbsRootPath, path)
+		}
+	})
+
+	t.Run("DefaultNameWinsWhenBothExist", func(t *testing.T) {
+		dir := t.TempDir()
+		jsonPath := filepath.Join(dir, configfile.DefaultName)
+		if err := os.WriteFile(jsonPath, []byte(`{"packages": []}`), 0o644); err != nil {
+			t.Fatal(err)
+		}
+		if err := os.WriteFile(filepath.Join(dir, configfile.AltName), []byte(jsonc), 0o644); err != nil {
+			t.Fatal(err)
+		}
+
+		cfg, err := Open(dir)
+		if err != nil {
+			t.Fatalf("Open(%q) error: %v", dir, err)
+		}
+		if cfg.Root.AbsRootPath != jsonPath {
+			t.Errorf("cfg.Root.AbsRootPath = %q, want %q", cfg.Root.AbsRootPath, jsonPath)
+		}
+	})
+
+	t.Run("SaveWritesBackToJSONC", func(t *testing.T) {
+		dir := t.TempDir()
+		path := filepath.Join(dir, configfile.AltName)
+		if err := os.WriteFile(path, []byte(jsonc), 0o644); err != nil {
+			t.Fatal(err)
+		}
+
+		cfg, err := Open(dir)
+		if err != nil {
+			t.Fatalf("Open(%q) error: %v", dir, err)
+		}
+		if err := cfg.Root.SaveTo(dir); err != nil {
+			t.Fatalf("SaveTo(%q) error: %v", dir, err)
+		}
+
+		// Saving must write back to devbox.jsonc, not create a devbox.json.
+		if _, err := os.Stat(filepath.Join(dir, configfile.DefaultName)); !errors.Is(err, fs.ErrNotExist) {
+			t.Errorf("SaveTo created a %s; want it to update %s in place",
+				configfile.DefaultName, configfile.AltName)
+		}
+		if _, err := os.Stat(path); err != nil {
+			t.Errorf("os.Stat(%q) after save: %v", path, err)
+		}
+	})
+}
+
 // mkNestedDirs sets up a nested directory structure for Find and Open tests.
 func mkNestedDirs(t *testing.T) (root, child, nested string) {
 	t.Helper()
@@ -599,3 +679,20 @@ func (p *testLockProject) ConfigHash() (string, error) { return "", nil }
 func (p *testLockProject) Stdenv() flake.Ref                                        { return flake.Ref{} }
 func (p *testLockProject) AllPackageNamesIncludingRemovedTriggerPackages() []string { return nil }
 func (p *testLockProject) ProjectDir() string                                       { return p.dir }
+
+func TestInitRefusesWhenJSONCExists(t *testing.T) {
+	dir := t.TempDir()
+	jsoncPath := filepath.Join(dir, configfile.AltName)
+	if err := os.WriteFile(jsoncPath, []byte("{\n  // comment\n  \"packages\": []\n}\n"), 0o644); err != nil {
+		t.Fatal(err)
+	}
+
+	_, err := Init(dir)
+	if !errors.Is(err, fs.ErrExist) {
+		t.Fatalf("Init() with existing %s: got err %v, want fs.ErrExist", configfile.AltName, err)
+	}
+	// Init must not have created a devbox.json that would shadow the jsonc.
+	if _, err := os.Stat(filepath.Join(dir, configfile.DefaultName)); !errors.Is(err, fs.ErrNotExist) {
+		t.Errorf("Init() created %s next to an existing %s", configfile.DefaultName, configfile.AltName)
+	}
+}
diff --git a/internal/devconfig/configfile/file.go b/internal/devconfig/configfile/file.go
index 1bf94a4c190..a5e81927feb 100644
--- a/internal/devconfig/configfile/file.go
+++ b/internal/devconfig/configfile/file.go
@@ -21,8 +21,19 @@ import (
 
 const (
 	DefaultName = "devbox.json"
+	// AltName is an alternate config filename that devbox also recognizes.
+	// devbox.json already permits comments (it is parsed as JSONC), but
+	// editors and GitHub diffs flag comments in a .json file as errors. Naming
+	// the file devbox.jsonc lets those tools highlight it correctly without any
+	// extra configuration. See https://github.com/jetify-com/devbox/issues/2602
+	AltName = "devbox.jsonc"
 )
 
+// ValidNames are the config filenames devbox recognizes, in the order they are
+// searched for within a directory. devbox.json is listed first so it wins when
+// a directory happens to contain both files.
+var ValidNames = []string{DefaultName, AltName}
+
 // ConfigFile defines a devbox environment as JSON.
 type ConfigFile struct {
 	// AbsRootPath is the absolute path to the devbox.json or plugin.json file
@@ -114,9 +125,21 @@ func (c *ConfigFile) InitHook() *shellcmd.Commands {
 	return c.Shell.InitHook
 }
 
-// SaveTo writes the config to a file.
-func (c *ConfigFile) SaveTo(path string) error {
-	return os.WriteFile(filepath.Join(path, DefaultName), c.Bytes(), 0o644)
+// FileName returns the base name of the config file (e.g. "devbox.json" or
+// "devbox.jsonc"). It preserves whatever name the config was loaded from so
+// that saving writes back to the same file. It falls back to [DefaultName] when
+// the config has no on-disk path (for example, a config loaded from a URL).
+func (c *ConfigFile) FileName() string {
+	if c.AbsRootPath != "" {
+		return filepath.Base(c.AbsRootPath)
+	}
+	return DefaultName
+}
+
+// SaveTo writes the config into the directory dir, using the config's original
+// filename (see [ConfigFile.FileName]).
+func (c *ConfigFile) SaveTo(dir string) error {
+	return os.WriteFile(filepath.Join(dir, c.FileName()), c.Bytes(), 0o644)
 }
 
 // TODO: Can we remove SaveTo and just use Save()?
diff --git a/internal/devconfig/configfile/file_test.go b/internal/devconfig/configfile/file_test.go
index c58f8a08086..66804c6e306 100644
--- a/internal/devconfig/configfile/file_test.go
+++ b/internal/devconfig/configfile/file_test.go
@@ -4,6 +4,8 @@ package configfile
 import (
 	"encoding/json"
 	"io"
+	"os"
+	"path/filepath"
 	"strings"
 	"testing"
 
@@ -782,3 +784,52 @@ func TestNixpkgsValidation(t *testing.T) {
 		})
 	}
 }
+
+func TestFileName(t *testing.T) {
+	testCases := map[string]struct {
+		absRootPath string
+		want        string
+	}{
+		"empty_falls_back_to_default": {"", DefaultName},
+		"json":                        {"/home/user/project/devbox.json", DefaultName},
+		"jsonc":                       {"/home/user/project/devbox.jsonc", AltName},
+	}
+
+	for name, testCase := range testCases {
+		t.Run(name, func(t *testing.T) {
+			c := &ConfigFile{AbsRootPath: testCase.absRootPath}
+			if got := c.FileName(); got != testCase.want {
+				t.Errorf("FileName() = %q, want %q", got, testCase.want)
+			}
+		})
+	}
+}
+
+func TestSaveToPreservesFileName(t *testing.T) {
+	testCases := map[string]struct {
+		absRootPath string
+		wantName    string
+	}{
+		"json":                 {"/anywhere/devbox.json", DefaultName},
+		"jsonc":                {"/anywhere/devbox.jsonc", AltName},
+		"no_path_uses_default": {"", DefaultName},
+	}
+
+	for name, testCase := range testCases {
+		t.Run(name, func(t *testing.T) {
+			in, err := LoadBytes([]byte(`{"packages": []}`))
+			if err != nil {
+				t.Fatalf("LoadBytes error: %v", err)
+			}
+			in.AbsRootPath = testCase.absRootPath
+
+			dir := t.TempDir()
+			if err := in.SaveTo(dir); err != nil {
+				t.Fatalf("SaveTo(%q) error: %v", dir, err)
+			}
+			if _, err := os.Stat(filepath.Join(dir, testCase.wantName)); err != nil {
+				t.Errorf("expected %q to be written: %v", testCase.wantName, err)
+			}
+		})
+	}
+}
diff --git a/internal/devconfig/init.go b/internal/devconfig/init.go
index 911ae3976be..fa3b59b2482 100644
--- a/internal/devconfig/init.go
+++ b/internal/devconfig/init.go
@@ -4,6 +4,7 @@
 package devconfig
 
 import (
+	"io/fs"
 	"os"
 	"path/filepath"
 
@@ -11,6 +12,16 @@ import (
 )
 
 func Init(dir string) (*Config, error) {
+	// A project may already be configured under an alternate filename
+	// (devbox.jsonc). Creating devbox.json next to it would silently take
+	// precedence, so treat any recognized config name as "already exists".
+	for _, name := range configfile.ValidNames {
+		path := filepath.Join(dir, name)
+		if _, err := os.Stat(path); err == nil {
+			return nil, &fs.PathError{Op: "open", Path: path, Err: fs.ErrExist}
+		}
+	}
+
 	file, err := os.OpenFile(
 		filepath.Join(dir, configfile.DefaultName),
 		os.O_RDWR|os.O_CREATE|os.O_EXCL,
diff --git a/internal/pullbox/files.go b/internal/pullbox/files.go
index 1f30ed9be92..12e2c886a9b 100644
--- a/internal/pullbox/files.go
+++ b/internal/pullbox/files.go
@@ -8,6 +8,7 @@ import (
 	"net/http"
 	"os"
 	"path/filepath"
+	"slices"
 	"strings"
 
 	"github.com/pkg/errors"
@@ -63,7 +64,7 @@ func profileIsNotEmpty(path string) (bool, error) {
 		return false, errors.WithStack(err)
 	}
 	for _, entry := range entries {
-		if entry.Name() != configfile.DefaultName ||
+		if !slices.Contains(configfile.ValidNames, entry.Name()) ||
 			isModifiedConfig(filepath.Join(path, entry.Name())) {
 			return true, nil
 		}
@@ -72,7 +73,7 @@ func profileIsNotEmpty(path string) (bool, error) {
 }
 
 func isModifiedConfig(path string) bool {
-	if filepath.Base(path) == configfile.DefaultName {
+	if slices.Contains(configfile.ValidNames, filepath.Base(path)) {
 		return !devconfig.IsDefault(path)
 	}
 	return false
diff --git a/testscripts/generate/direnv-config-envflag.test.txt b/testscripts/generate/direnv-config-envflag.test.txt
index dc5c9194b04..ea38393d78c 100644
--- a/testscripts/generate/direnv-config-envflag.test.txt
+++ b/testscripts/generate/direnv-config-envflag.test.txt
@@ -20,7 +20,7 @@ cmp stdout ../expected-results.txt
 -- expected-results.txt --
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias --env x=y )"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 
diff --git a/testscripts/generate/direnv-config.test.txt b/testscripts/generate/direnv-config.test.txt
index 0211b3ff4ec..6ab07c4dabb 100644
--- a/testscripts/generate/direnv-config.test.txt
+++ b/testscripts/generate/direnv-config.test.txt
@@ -20,7 +20,7 @@ cmp stdout ../expected-results.txt
 -- expected-results.txt --
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias)"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 
diff --git a/testscripts/generate/direnv-envflag.test.txt b/testscripts/generate/direnv-envflag.test.txt
index 2dd0aea9ff5..10b069e7c8f 100644
--- a/testscripts/generate/direnv-envflag.test.txt
+++ b/testscripts/generate/direnv-envflag.test.txt
@@ -15,7 +15,7 @@ cmp stdout expected-results.txt
 -- expected-results.txt --
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias --env x=y )"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 
diff --git a/testscripts/generate/direnv-envrcdir-config-parent.test.txt b/testscripts/generate/direnv-envrcdir-config-parent.test.txt
index 161e14dff83..ff62cfc6ab8 100644
--- a/testscripts/generate/direnv-envrcdir-config-parent.test.txt
+++ b/testscripts/generate/direnv-envrcdir-config-parent.test.txt
@@ -21,7 +21,7 @@ cmp stdout ../expected-results.txt
 -- expected-results.txt --
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias)"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 
diff --git a/testscripts/generate/direnv-envrcdir-config-sibling.test.txt b/testscripts/generate/direnv-envrcdir-config-sibling.test.txt
index 0e48471de7b..bf8a55062e3 100644
--- a/testscripts/generate/direnv-envrcdir-config-sibling.test.txt
+++ b/testscripts/generate/direnv-envrcdir-config-sibling.test.txt
@@ -19,7 +19,7 @@ cmp stdout ../expected-results.txt
 -- expected-results.txt --
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias --config ../cfg)"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 
diff --git a/testscripts/generate/direnv-envrcdir-config-subdir-envflag.test.txt b/testscripts/generate/direnv-envrcdir-config-subdir-envflag.test.txt
index 2dcab6115e1..61bab2e5dd1 100644
--- a/testscripts/generate/direnv-envrcdir-config-subdir-envflag.test.txt
+++ b/testscripts/generate/direnv-envrcdir-config-subdir-envflag.test.txt
@@ -18,7 +18,7 @@ cmp stdout ../expected-results.txt
 -- expected-results.txt --
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias --env x=y  --config cfg)"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 
diff --git a/testscripts/generate/direnv-envrcdir-config-subdir.test.txt b/testscripts/generate/direnv-envrcdir-config-subdir.test.txt
index 83dbcd001fd..c7fba91c595 100644
--- a/testscripts/generate/direnv-envrcdir-config-subdir.test.txt
+++ b/testscripts/generate/direnv-envrcdir-config-subdir.test.txt
@@ -18,7 +18,7 @@ cmp stdout ../expected-results.txt
 -- expected-results.txt --
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias --config cfg)"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 
diff --git a/testscripts/generate/direnv-envrcdir-current-config-sub.test.txt b/testscripts/generate/direnv-envrcdir-current-config-sub.test.txt
index 0d6533486b7..ea5aabf8206 100644
--- a/testscripts/generate/direnv-envrcdir-current-config-sub.test.txt
+++ b/testscripts/generate/direnv-envrcdir-current-config-sub.test.txt
@@ -17,7 +17,7 @@ cmp stdout expected-results.txt
 -- expected-results.txt --
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias --config cfg)"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 
diff --git a/testscripts/generate/direnv-envrcdir-parent.test.txt b/testscripts/generate/direnv-envrcdir-parent.test.txt
index a49a6424a93..4bc2c3ade3c 100644
--- a/testscripts/generate/direnv-envrcdir-parent.test.txt
+++ b/testscripts/generate/direnv-envrcdir-parent.test.txt
@@ -20,7 +20,7 @@ cmp stdout expected-results.txt
 -- expected-results.txt --
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias --config cfg)"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 
diff --git a/testscripts/generate/direnv-envrcdir.test.txt b/testscripts/generate/direnv-envrcdir.test.txt
index 43cae344ce5..82dd4bc96d9 100644
--- a/testscripts/generate/direnv-envrcdir.test.txt
+++ b/testscripts/generate/direnv-envrcdir.test.txt
@@ -21,7 +21,7 @@ cmp stdout ../expected-results.txt
 -- expected-results.txt --
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias)"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 
diff --git a/testscripts/generate/direnv-printenvrc-config.test.txt b/testscripts/generate/direnv-printenvrc-config.test.txt
index 89182a07f2c..72d6f917bdf 100644
--- a/testscripts/generate/direnv-printenvrc-config.test.txt
+++ b/testscripts/generate/direnv-printenvrc-config.test.txt
@@ -15,7 +15,7 @@ cmp stdout expected-results.txt
 -- expected-results.txt --
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias --config config-dir)"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 
diff --git a/testscripts/generate/direnv-printenvrc.test.txt b/testscripts/generate/direnv-printenvrc.test.txt
index 9c66cda6302..b4f6546ded5 100644
--- a/testscripts/generate/direnv-printenvrc.test.txt
+++ b/testscripts/generate/direnv-printenvrc.test.txt
@@ -14,7 +14,7 @@ cmp stdout expected-results.txt
 -- expected-results.txt --
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias)"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 
diff --git a/testscripts/generate/direnv.test.txt b/testscripts/generate/direnv.test.txt
index f09a0d2b893..3885802fe8b 100644
--- a/testscripts/generate/direnv.test.txt
+++ b/testscripts/generate/direnv.test.txt
@@ -15,7 +15,7 @@ cmp stdout expected-results.txt
 -- expected-results.txt --
 use_devbox() {
     eval "$(devbox shellenv --init-hook --install --no-refresh-alias)"
-    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.lock
+    watch_file $DEVBOX_PROJECT_ROOT/devbox.json $DEVBOX_PROJECT_ROOT/devbox.jsonc $DEVBOX_PROJECT_ROOT/devbox.lock
 }
 use devbox
 
diff --git a/testscripts/init/empty.test.txt b/testscripts/init/empty.test.txt
index 74f9b0ce00a..6c64a6b6d47 100644
--- a/testscripts/init/empty.test.txt
+++ b/testscripts/init/empty.test.txt
@@ -8,7 +8,7 @@ json.superset devbox.json expected.json
 
 # Second init should be a no-op with a warning
 exec devbox init
-stderr 'devbox.json already exists in'
+stderr 'A devbox config already exists in'
 
 -- expected.json --
 {