diff --git a/pontoon/administration/forms.py b/pontoon/administration/forms.py
index b549daf643..1f9b16989f 100644
--- a/pontoon/administration/forms.py
+++ b/pontoon/administration/forms.py
@@ -38,9 +38,10 @@ class ProjectForm(forms.ModelForm):
 
     def clean(self):
         cleaned_data = super().clean()
+        set_locales_from_repo = cleaned_data.get("set_locales_from_repo")
         locales_readonly = cleaned_data.get("locales_readonly")
         locales = cleaned_data.get("locales")
-        if not (locales or locales_readonly):
+        if not (set_locales_from_repo or locales or locales_readonly):
             raise ValidationError("At least one locale must be selected.")
 
     class Meta:
@@ -61,6 +62,8 @@ class Meta:
             "sync_disabled",
             "tags_enabled",
             "pretranslation_enabled",
+            "set_locales_from_repo",
+            "set_translated_resources_from_repo",
             "visibility",
         )
 
diff --git a/pontoon/administration/static/css/admin_project.css b/pontoon/administration/static/css/admin_project.css
index ad3ba79a78..0e3a5ad86e 100644
--- a/pontoon/administration/static/css/admin_project.css
+++ b/pontoon/administration/static/css/admin_project.css
@@ -178,12 +178,20 @@ form a:visited {
   margin: 5px 9px;
 }
 
+.controls .save {
+  width: 150px !important;
+}
+
 .controls .checkbox {
   float: left;
   margin: -1px 20px 0 0;
   text-transform: uppercase;
 }
 
+.locales {
+  margin-top: 40px;
+}
+
 .double-list-selector .locale.select .menu {
   background: transparent;
   border-bottom: 1px solid var(--main-border-1);
diff --git a/pontoon/administration/static/js/admin_project.js b/pontoon/administration/static/js/admin_project.js
index 4b19493a2d..0c096873be 100644
--- a/pontoon/administration/static/js/admin_project.js
+++ b/pontoon/administration/static/js/admin_project.js
@@ -76,8 +76,9 @@ $(function () {
 
     button.addClass('in-progress').html('Syncing...');
 
+    const slug = $('#id_slug').val();
     $.ajax({
-      url: '/admin/projects/' + $('#id_slug').val() + '/sync/',
+      url: `/admin/projects/${slug}/sync/`,
       success: function () {
         button.html('Started');
       },
@@ -105,8 +106,9 @@ $(function () {
 
     button.addClass('in-progress').html('Pretranslating...');
 
+    const slug = $('#id_slug').val();
     $.ajax({
-      url: '/admin/projects/' + $('#id_slug').val() + '/pretranslate/',
+      url: `/admin/projects/${slug}/pretranslate/`,
       success: function () {
         button.html('Started');
       },
@@ -166,6 +168,51 @@ $(function () {
     });
   });
 
+  const setLocalesCheckbox = $('#id_set_locales_from_repo');
+  const configFileInput = $('#id_configuration_file');
+  function setLocalesUpdate() {
+    const configFile = configFileInput.val();
+    let reqSync = configFile !== configFileInput.data('init');
+
+    const controls = $('.repo-locale-control');
+    if ($('#id_data_source').val() === 'repository') {
+      controls.show();
+    } else {
+      controls.hide();
+      setLocalesCheckbox.prop('checked', false);
+      reqSync = false;
+    }
+
+    const label = $('#id_set_locales_from_repo + span');
+    const hint = $('#hint_set_locales_from_repo');
+    if (configFile) {
+      label.text('Read locales from configuration file');
+      hint.hide();
+    } else {
+      label.text('Set locales from repository');
+      hint.show();
+    }
+
+    const setLocalesFromRepo = setLocalesCheckbox.prop('checked');
+    const trDiv = $('#translated_resources_from_repo');
+    const locales = $('.locales, .locales-toolbar');
+    if (setLocalesFromRepo) {
+      trDiv.toggle(!configFile);
+      locales.hide();
+      reqSync ||= setLocalesFromRepo !== setLocalesCheckbox.data('init');
+    } else {
+      trDiv.hide();
+      locales.show();
+    }
+
+    $('button.save').text(reqSync ? 'Save & sync project' : 'Save project');
+  }
+  setLocalesCheckbox.data('init', setLocalesCheckbox.prop('checked'));
+  setLocalesCheckbox.on('change', setLocalesUpdate);
+  configFileInput.data('init', configFileInput.val());
+  configFileInput.on('change', setLocalesUpdate);
+  setLocalesUpdate();
+
   self.NProgressUnbind();
 
   // Set locales to existing projects to be copied to the current project
diff --git a/pontoon/administration/templates/admin_project.html b/pontoon/administration/templates/admin_project.html
index 55dfcddaff..cbcd143f02 100644
--- a/pontoon/administration/templates/admin_project.html
+++ b/pontoon/administration/templates/admin_project.html
@@ -54,7 +54,29 @@ <h1>
 
     <h3>Locales</h3>
 
-    <div class="locales clearfix">
+    <div class="repo-locale-control checkbox clearfix">
+      <label for="id_set_locales_from_repo">
+        {{ form.set_locales_from_repo }}
+        <span></span>
+      </label>
+      <span id="hint_set_locales_from_repo"
+        >Locale is available if target directory is present.</span
+      >
+    </div>
+
+    <div
+      class="repo-locale-control checkbox clearfix"
+      id="translated_resources_from_repo"
+      style="display: none"
+    >
+      <label for="id_set_translated_resources_from_repo">
+        {{ form.set_translated_resources_from_repo }} Set per-resource
+        localizability from repository
+      </label>
+      Resource is available if target file is present in locale directory.
+    </div>
+
+    <div class="locales clearfix" style="display: none">
       {{ admin_team_selector.render(locales_available, locales_selected, locales_readonly) }}
       {{ form.locales }}
       {{ form.locales.errors }}
diff --git a/pontoon/administration/views.py b/pontoon/administration/views.py
index 62756ef97e..d673bb4904 100644
--- a/pontoon/administration/views.py
+++ b/pontoon/administration/views.py
@@ -1,6 +1,8 @@
 import csv
 import logging
 
+from typing import cast
+
 from django.conf import settings
 from django.contrib.auth.decorators import login_required
 from django.core.exceptions import PermissionDenied
@@ -33,6 +35,8 @@
 from pontoon.pretranslation.tasks import pretranslate_task
 from pontoon.sync.tasks import sync_project_task
 
+from ..base.models.project import ProjectQuerySet
+
 
 log = logging.getLogger(__name__)
 
@@ -127,6 +131,8 @@ def manage_project(request, slug=None, template="admin_project.html"):
     subtitle = "Add project"
     pk = None
     project = None
+    prev_config_file = None
+    prev_set_locales_from_repo = False
 
     # Save project
     if request.method == "POST":
@@ -143,7 +149,11 @@ def manage_project(request, slug=None, template="admin_project.html"):
         # Update existing project
         try:
             pk = request.POST["pk"]
-            project = Project.objects.visible_for(request.user).get(pk=pk)
+            project = (
+                cast(ProjectQuerySet, Project.objects)
+                .visible_for(request.user)
+                .get(pk=pk)
+            )
             form = ProjectForm(request.POST, instance=project)
             # Needed if form invalid
             repo_formset = RepositoryInlineFormSet(request.POST, instance=project)
@@ -156,6 +166,8 @@ def manage_project(request, slug=None, template="admin_project.html"):
                 request.POST, instance=project
             )
             subtitle = "Edit project"
+            prev_config_file = project.configuration_file
+            prev_set_locales_from_repo = project.set_locales_from_repo
 
         # Add a new project
         except MultiValueDictKeyError:
@@ -166,7 +178,7 @@ def manage_project(request, slug=None, template="admin_project.html"):
             tag_formset = None
 
         if form.is_valid():
-            project = form.save(commit=False)
+            project = cast(Project, form.save(commit=False))
             repo_formset = RepositoryInlineFormSet(request.POST, instance=project)
             external_resource_formset = ExternalResourceInlineFormSet(
                 request.POST, instance=project
@@ -180,38 +192,43 @@ def manage_project(request, slug=None, template="admin_project.html"):
             )
             if formsets_valid:
                 project.save()
-
-                # Manually save ProjectLocales due to intermediary model
-                locales_form = form.cleaned_data.get("locales", [])
-                locales_readonly_form = form.cleaned_data.get("locales_readonly", [])
-                locales = locales_form | locales_readonly_form
-
-                (
-                    ProjectLocale.objects.filter(project=project)
-                    .exclude(locale__pk__in=[loc.pk for loc in locales])
-                    .delete()
-                )
-
-                for locale in locales:
-                    # The implicit pre_save and post_save signals sent here are required
-                    # to maintain django-guardian permissions.
-                    ProjectLocale.objects.get_or_create(project=project, locale=locale)
-
-                project_locales = ProjectLocale.objects.filter(project=project)
-
-                # Update readonly flags
-                locales_readonly_pks = [loc.pk for loc in locales_readonly_form]
-                project_locales.filter(readonly=True).exclude(
-                    locale__pk__in=locales_readonly_pks
-                ).update(readonly=False)
-                project_locales.filter(
-                    locale__pk__in=locales_readonly_pks, readonly=False
-                ).update(readonly=True)
+                pk = project.pk
+                data = form.cleaned_data
+
+                set_locales_from_repo = data.get("set_locales_from_repo", False)
+
+                if set_locales_from_repo:
+                    project_locales = ProjectLocale.objects.filter(project=project)
+                else:
+                    # Manually save ProjectLocales due to intermediary model
+                    locales_form = data.get("locales", set())
+                    locales_readonly_form = data.get("locales_readonly", set())
+                    locales = locales_form | locales_readonly_form
+
+                    ProjectLocale.objects.filter(project=project).exclude(
+                        locale__pk__in=[loc.pk for loc in locales]
+                    ).delete()
+
+                    for locale in locales:
+                        # The implicit pre_save and post_save signals sent here are required
+                        # to maintain django-guardian permissions.
+                        ProjectLocale.objects.get_or_create(
+                            project=project, locale=locale
+                        )
+
+                    project_locales = ProjectLocale.objects.filter(project=project)
+
+                    # Update readonly flags
+                    locales_readonly_pks = [loc.pk for loc in locales_readonly_form]
+                    project_locales.filter(readonly=True).exclude(
+                        locale__pk__in=locales_readonly_pks
+                    ).update(readonly=False)
+                    project_locales.filter(
+                        locale__pk__in=locales_readonly_pks, readonly=False
+                    ).update(readonly=True)
 
                 # Update pretranslate flags
-                locales_pretranslate_form = form.cleaned_data.get(
-                    "locales_pretranslate", []
-                )
+                locales_pretranslate_form = data.get("locales_pretranslate", [])
                 locales_pretranslate_pks = [loc.pk for loc in locales_pretranslate_form]
                 project_locales.filter(pretranslation_enabled=True).exclude(
                     locale__pk__in=locales_pretranslate_pks,
@@ -239,7 +256,14 @@ def manage_project(request, slug=None, template="admin_project.html"):
                 if project.tags_enabled:
                     tag_formset = TagInlineFormSet(instance=project)
                 subtitle += ". Saved."
-                pk = project.pk
+
+                if project.data_source == Project.DataSource.REPOSITORY and (
+                    set_locales_from_repo
+                    and not prev_set_locales_from_repo
+                    or data.get("configuration_file") != prev_config_file
+                ):
+                    sync_project_task.delay(project.pk)
+                    subtitle += " Sync started."
             else:
                 subtitle += ". Error."
         else:
diff --git a/pontoon/base/migrations/0119_project_set_locales_from_repo_and_more.py b/pontoon/base/migrations/0119_project_set_locales_from_repo_and_more.py
new file mode 100644
index 0000000000..b25855c61c
--- /dev/null
+++ b/pontoon/base/migrations/0119_project_set_locales_from_repo_and_more.py
@@ -0,0 +1,28 @@
+# Generated by Django 5.2.14 on 2026-06-24 09:50
+
+from django.db import migrations, models
+
+
+class Migration(migrations.Migration):
+    dependencies = [
+        ("base", "0118_fix_terminology_entity_value"),
+    ]
+
+    operations = [
+        migrations.AddField(
+            model_name="project",
+            name="set_locales_from_repo",
+            field=models.BooleanField(
+                default=False,
+                help_text="\n        Control target locales by their directories' presence in the target repository,\n        or in the root locales config if `configuration_file` is not None.\n        ",
+            ),
+        ),
+        migrations.AddField(
+            model_name="project",
+            name="set_translated_resources_from_repo",
+            field=models.BooleanField(
+                default=False,
+                help_text="\n        If `set_locales_from_repo` is True and `configuration_file` is None,\n        setting `set_translated_resources_from_repo` to True will\n        control the availability of each resource for translation in each locale\n        according to the presence of a file (even if empty) at its expected target path.\n\n        If `set_locales_from_repo` is False or `configuration_file` is not None,\n        this control has no effect.\n        ",
+            ),
+        ),
+    ]
diff --git a/pontoon/base/models/project.py b/pontoon/base/models/project.py
index 574ce8b77e..62f6af023e 100644
--- a/pontoon/base/models/project.py
+++ b/pontoon/base/models/project.py
@@ -237,6 +237,27 @@ class Visibility(models.TextChoices):
         """,
     )
 
+    set_locales_from_repo = models.BooleanField(
+        default=False,
+        help_text="""
+        Control target locales by their directories' presence in the target repository,
+        or in the root locales config if `configuration_file` is not None.
+        """,
+    )
+
+    set_translated_resources_from_repo = models.BooleanField(
+        default=False,
+        help_text="""
+        If `set_locales_from_repo` is True and `configuration_file` is None,
+        setting `set_translated_resources_from_repo` to True will
+        control the availability of each resource for translation in each locale
+        according to the presence of a file (even if empty) at its expected target path.
+
+        If `set_locales_from_repo` is False or `configuration_file` is not None,
+        this control has no effect.
+        """,
+    )
+
     objects = ProjectQuerySet.as_manager()
 
     project_locale: "ProjectLocaleQuerySet"
diff --git a/pontoon/sync/core/__init__.py b/pontoon/sync/core/__init__.py
index 84b30101f9..4506d3f49d 100644
--- a/pontoon/sync/core/__init__.py
+++ b/pontoon/sync/core/__init__.py
@@ -11,6 +11,7 @@
     Entity,
     Locale,
     Project,
+    ProjectLocale,
     TranslatedResource,
     Translation,
     User,
@@ -50,10 +51,30 @@ def sync_project(
         log.error(f"{log_prefix} {e}")
         raise e
 
-    locale_map: dict[str, Locale] = {
-        lc.code: lc for lc in project.locales.order_by("code")
-    }
+    locale_map: dict[str, Locale]
+    if project.set_locales_from_repo:
+        if not paths.locales:
+            errmsg = "No locales found in repo"
+            log.error(f"{log_prefix} {errmsg}")
+            raise Exception(errmsg)
+        locales = Locale.objects.filter(code__in=paths.locales).order_by("code")
+        locale_map = {lc.code: lc for lc in locales}
+
+        # Update project locales
+        ProjectLocale.objects.filter(project=project).exclude(
+            locale__in=locales
+        ).delete()
+        for locale in locales:
+            # The implicit pre_save and post_save signals sent here are required
+            # to maintain django-guardian permissions.
+            ProjectLocale.objects.get_or_create(project=project, locale=locale)
+        ProjectLocale.objects.filter(project=project, readonly=True).update(
+            readonly=False
+        )
+    else:
+        locale_map = {lc.code: lc for lc in project.locales.order_by("code")}
     paths.locales = list(locale_map.keys())
+
     added_entities_count, changed_paths, removed_paths = sync_resources_from_repo(
         project, locale_map, checkouts.source, paths, now
     )
diff --git a/pontoon/sync/core/entities.py b/pontoon/sync/core/entities.py
index f92df4cf09..d2957ba551 100644
--- a/pontoon/sync/core/entities.py
+++ b/pontoon/sync/core/entities.py
@@ -375,7 +375,7 @@ def update_translated_resources(
         _, locales = paths.target(resource.path)
         for lc in locales:
             locale = locale_map.get(lc, None)
-            if is_translated_resource(paths, resource, locale):
+            if is_translated_resource(project, paths, resource, locale):
                 assert locale is not None
                 key = (resource.pk, locale.pk)
                 if key in prev_tr_keys:
@@ -403,6 +403,7 @@ def update_translated_resources(
 
 
 def is_translated_resource(
+    project: Project,
     paths: L10nConfigPaths | L10nDiscoverPaths,
     resource: Resource,
     locale: Locale | None,
@@ -410,9 +411,13 @@ def is_translated_resource(
     if locale is None:
         return False
 
-    if resource.format == Resource.Format.GETTEXT:
-        # For gettext, only create TranslatedResource
-        # if the resource exists for the locale.
+    if (
+        isinstance(paths, L10nDiscoverPaths)
+        and project.set_locales_from_repo
+        and project.set_translated_resources_from_repo
+    ):
+        # With `set_translated_resources_from_repo`,
+        # only create TranslatedResource if the resource exists for the locale.
         target, _ = paths.target(resource.path)
         if target is None:
             return False
diff --git a/pontoon/sync/core/translations_from_repo.py b/pontoon/sync/core/translations_from_repo.py
index a785ebb122..760da10413 100644
--- a/pontoon/sync/core/translations_from_repo.py
+++ b/pontoon/sync/core/translations_from_repo.py
@@ -53,7 +53,15 @@ def sync_translations_from_repo(
     """(removed_resource_count, updated_translation_count)"""
     co = checkouts.target
     source_paths: set[str] = set(paths.ref_paths) if checkouts.source == co else set()
-    del_count = delete_removed_gettext_resources(project, co, paths, source_paths)
+    del_count = (
+        delete_removed_resources(project, co, paths, source_paths)
+        if (
+            isinstance(paths, L10nDiscoverPaths)
+            and project.set_locales_from_repo
+            and project.set_translated_resources_from_repo
+        )
+        else 0
+    )
 
     changed_target_paths = [
         path
@@ -83,10 +91,10 @@ def write_db_updates(
     add_translation_memory_entries(project, new_translations + updated_translations)
 
 
-def delete_removed_gettext_resources(
+def delete_removed_resources(
     project: Project,
     target: Checkout,
-    paths: L10nConfigPaths | L10nDiscoverPaths,
+    paths: L10nDiscoverPaths,
     source_paths: set[str],
 ) -> int:
     rm_t = Q()
@@ -95,7 +103,7 @@ def delete_removed_gettext_resources(
     removed_target_paths = (
         path
         for path in (join(target.path, co_path) for co_path in target.removed)
-        if path not in source_paths and splitext(path)[1] in {".po", ".pot"}
+        if path not in source_paths
     )
     for target_path in removed_target_paths:
         ref = paths.find_reference(target_path)
@@ -104,7 +112,7 @@ def delete_removed_gettext_resources(
             locale_code = get_path_locale(path_vars)
             if locale_code is not None:
                 db_path = relpath(ref_path, paths.ref_root)
-                if not project.configuration_file and db_path.endswith(".pot"):
+                if db_path.endswith(".pot"):
                     db_path = db_path[:-1]
                 rm_t |= Q(entity__resource__path=db_path, locale__code=locale_code)
                 rm_tr |= Q(resource__path=db_path, locale__code=locale_code)
diff --git a/pontoon/sync/tests/test_e2e.py b/pontoon/sync/tests/test_e2e.py
index 0327a045ef..4d8e4523bf 100644
--- a/pontoon/sync/tests/test_e2e.py
+++ b/pontoon/sync/tests/test_e2e.py
@@ -17,6 +17,7 @@
     ChangedEntityLocale,
     Entity,
     Locale,
+    ProjectLocale,
     Repository,
     TranslatedResource,
     Translation,
@@ -242,7 +243,11 @@ def test_add_resources():
         assert {
             (tr.resource.path, tr.locale.code)
             for tr in TranslatedResource.objects.filter(resource__project=project)
-        } == {("file.ftl", "de-Test"), ("file.xliff", "de-Test")}
+        } == {
+            ("file.ftl", "de-Test"),
+            ("file.po", "de-Test"),
+            ("file.xliff", "de-Test"),
+        }
 
         # Add an XLIFF translation
         TranslationFactory.create(
@@ -848,3 +853,82 @@ def test_add_project_locale():
             tr.locale.code: tr.total_strings
             for tr in TranslatedResource.objects.filter(resource__project=project)
         } == {"fr-Test": 1, "de-Test": 1}
+
+
+@pytest.mark.django_db
+def test_locales_from_repo():
+    mock_vcs = MockVersionControl(changed=[])
+    with mock_setup(mock_vcs) as (repo, _):
+        LocaleFactory.create(code="fr-Test", name="Test French")
+
+        # Database setup
+        project = ProjectFactory.create(
+            name="test-repo-locales",
+            locales=[],
+            repositories=[repo],
+            set_locales_from_repo=True,
+            system_project=False,
+        )
+
+        # Filesystem setup
+        makedirs(repo.checkout_path)
+        build_file_tree(
+            repo.checkout_path,
+            {
+                "en-US": {"messages.json": '{ "key": { "message": "Entity" } }'},
+                "de-Test": {"messages.json": "{}"},
+                "fr-Test": {"messages.json": "{}"},
+            },
+        )
+
+        sync_project_task(project.pk)
+
+        assert {
+            pl.locale.code for pl in ProjectLocale.objects.filter(project=project)
+        } == {"de-Test", "fr-Test"}
+        assert {
+            tr.locale.code: tr.total_strings
+            for tr in TranslatedResource.objects.filter(resource__project=project)
+        } == {"fr-Test": 1, "de-Test": 1}
+
+
+@pytest.mark.django_db
+def test_locales_from_config():
+    mock_vcs = MockVersionControl(changed=[])
+    with mock_setup(mock_vcs) as (repo, _):
+        LocaleFactory.create(code="fr-Test", name="Test French")
+
+        # Database setup
+        project = ProjectFactory.create(
+            name="test-config-locales",
+            configuration_file="l10n.toml",
+            locales=[],
+            repositories=[repo],
+            set_locales_from_repo=True,
+            system_project=False,
+        )
+
+        # Filesystem setup
+        makedirs(repo.checkout_path)
+        build_file_tree(
+            repo.checkout_path,
+            {
+                "foo": {"en": {"messages.json": '{ "key": { "message": "Entity" } }'}},
+                "l10n.toml": dedent("""\
+                    locales = ["de-Test", "fr-Test"]
+                    [[paths]]
+                        reference = "foo/en/**"
+                        l10n = "foo/{locale}/**"
+                    """),
+            },
+        )
+
+        sync_project_task(project.pk)
+
+        assert {
+            pl.locale.code for pl in ProjectLocale.objects.filter(project=project)
+        } == {"de-Test", "fr-Test"}
+        assert {
+            tr.locale.code: tr.total_strings
+            for tr in TranslatedResource.objects.filter(resource__project=project)
+        } == {"fr-Test": 1, "de-Test": 1}
diff --git a/pontoon/sync/tests/test_translations_from_repo.py b/pontoon/sync/tests/test_translations_from_repo.py
index bfc7ce6558..aa5bacd91e 100644
--- a/pontoon/sync/tests/test_translations_from_repo.py
+++ b/pontoon/sync/tests/test_translations_from_repo.py
@@ -358,6 +358,8 @@ def test_remove_po_target_resource():
             name="test-rm-po",
             locales=[locale],
             repositories=[repo],
+            set_locales_from_repo=True,
+            set_translated_resources_from_repo=True,
             visibility="public",
         )
         res = {}