diff --git a/internal/devbox/packages.go b/internal/devbox/packages.go
index 6c8d7319e75..9c7dd9a7c15 100644
--- a/internal/devbox/packages.go
+++ b/internal/devbox/packages.go
@@ -133,6 +133,15 @@ func (d *Devbox) Add(ctx context.Context, pkgsNames []string, opts devopt.AddOpt
 			// about not building on the current system, since user's can continue
 			// via --exclude-platform flag.
 			packageNameForConfig = pkg.Versioned()
+		} else if errors.Is(err, nix.ErrPackageNotFound) &&
+			versionedPkg.IsDevboxPackage &&
+			!strings.Contains(pkg.CanonicalName(), ".") {
+			// Heuristic: search indexes top-level nixpkgs packages, so falling
+			// back to nixpkgs (which requires a slow download) won't find it
+			// either. Nested attribute paths (e.g. stdenv.cc.cc.lib, openssl.dev,
+			// python3Packages.requests) are not all indexed, so those still fall
+			// back below.
+			return packageNotFoundError(pkg)
 		} else if !versionedPkg.IsDevboxPackage {
 			// This means it didn't validate and we don't want to fallback to legacy
 			// Just propagate the error.
@@ -146,7 +155,7 @@ func (d *Devbox) Add(ctx context.Context, pkgsNames []string, opts devopt.AddOpt
 			if err != nil {
 				// This means it looked like a devbox package or attribute path, but we
 				// could not find it in search or in the legacy nixpkgs path.
-				return usererr.New("Package %s not found", pkg.Raw)
+				return packageNotFoundError(pkg)
 			}
 		}
 
@@ -171,6 +180,13 @@ func (d *Devbox) Add(ctx context.Context, pkgsNames []string, opts devopt.AddOpt
 	return d.printPostAddMessage(ctx, pkgs, unchangedPackageNames, opts)
 }
 
+func packageNotFoundError(pkg *devpkg.Package) error {
+	return usererr.New(
+		"Package %q not found. To search for packages, use `devbox search %s`",
+		pkg.Raw, pkg.CanonicalName(),
+	)
+}
+
 func (d *Devbox) setPackageOptions(pkgs []string, opts devopt.AddOpts) error {
 	for _, pkg := range pkgs {
 		if err := d.cfg.PackageMutator().AddPlatforms(
diff --git a/internal/lock/resolve.go b/internal/lock/resolve.go
index 2183d7c6024..402b6f16618 100644
--- a/internal/lock/resolve.go
+++ b/internal/lock/resolve.go
@@ -68,9 +68,12 @@ func (f *File) FetchResolvedPackage(pkg string, refresh bool) (*Package, error)
 	}
 
 	packageVersion, err := searcher.Client().Resolve(name, version)
-	if err != nil {
+	if errors.Is(err, searcher.ErrNotFound) {
 		return nil, errors.Wrapf(nix.ErrPackageNotFound, "%s@%s", name, version)
 	}
+	if err != nil {
+		return nil, err
+	}
 
 	sysInfos, err := buildLockSystemInfos(packageVersion)
 	if err != nil {
diff --git a/internal/lock/resolve_test.go b/internal/lock/resolve_test.go
new file mode 100644
index 00000000000..12b3efe6117
--- /dev/null
+++ b/internal/lock/resolve_test.go
@@ -0,0 +1,43 @@
+// Copyright 2024 Jetify Inc. and contributors. All rights reserved.
+// Use of this source code is governed by the license in the LICENSE file.
+
+package lock
+
+import (
+	"errors"
+	"net/http"
+	"net/http/httptest"
+	"testing"
+
+	"go.jetify.com/devbox/internal/envir"
+	"go.jetify.com/devbox/internal/nix"
+)
+
+func TestFetchResolvedPackageErrors(t *testing.T) {
+	for _, resolveV2 := range []string{"0", "1"} {
+		for _, test := range []struct {
+			status       int
+			wantNotFound bool
+		}{
+			{http.StatusNotFound, true},
+			{http.StatusInternalServerError, false},
+		} {
+			t.Run("v2="+resolveV2+"/"+http.StatusText(test.status), func(t *testing.T) {
+				srv := httptest.NewServer(http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
+					w.WriteHeader(test.status)
+				}))
+				t.Cleanup(srv.Close)
+				t.Setenv(envir.DevboxSearchHost, srv.URL)
+				t.Setenv("DEVBOX_FEATURE_RESOLVE_V2", resolveV2)
+
+				_, err := (&File{}).FetchResolvedPackage("hello@latest", false)
+				if err == nil {
+					t.Fatal("got nil error, want an error")
+				}
+				if got := errors.Is(err, nix.ErrPackageNotFound); got != test.wantNotFound {
+					t.Errorf("errors.Is(err, nix.ErrPackageNotFound) = %v, want %v (err: %v)", got, test.wantNotFound, err)
+				}
+			})
+		}
+	}
+}
diff --git a/testscripts/add/add_not_found.test.txt b/testscripts/add/add_not_found.test.txt
new file mode 100644
index 00000000000..a690c52f2da
--- /dev/null
+++ b/testscripts/add/add_not_found.test.txt
@@ -0,0 +1,20 @@
+# Testscript for adding a package that doesn't exist.
+
+exec devbox init
+
+# A bare name that search doesn't know should fail fast without
+# downloading nixpkgs.
+! exec devbox add inotifywait
+stderr 'Package "inotifywait" not found. To search for packages, use `devbox search inotifywait`'
+! stderr 'Ensuring nixpkgs registry is downloaded'
+
+# The search hint drops the version.
+! exec devbox add hello@99999
+stderr 'Package "hello@99999" not found. To search for packages, use `devbox search hello`'
+
+json.superset devbox.json expected_devbox.json
+
+-- expected_devbox.json --
+{
+  "packages": []
+}