As suggested in the comments by e4c5, I changed my appoach massivly.
I now have a model with a FilerFolderField (still not documented) and a sortedm2m for filer.models.Image with a custom queryset of all files in the selected folder.
models.py:
class Car(models.Model):
    …
    folder = filer.fields.folder.FilerFolderField(blank=False)
    images = SortedManyToManyField(filer.models.Image)
    …
admin.py:
class CarAdminForm(ModelForm):
class Meta:
    model = Car
    fields = '__all__'
def __init__(self, *args, **kwargs):
    super(CarAdminForm, self).__init__(*args, **kwargs)
    choices = []
    for i in self.instance.folder.files.all():
        i.__str__ = thumb_string
        choices.append(i)
    self.fields['images'].queryset = self.instance.folder.files.all()
class CarAdmin(admin.ModelAdmin):
    list_display = ['name']
    list_filter = ['created']
    def __init__(self, model, admin_site):
        super(CarAdmin, self).__init__(model, admin_site)
        self.orig_form = self.form
    def change_view(self, request, object_id, form_url='',     extra_context=None):
        self.form = CarAdminForm
        self.prepopulated_fields = {}
        self.exclude = []
        return super(CarAdmin, self).change_view(request, object_id)
    def add_view(self, request, form_url='', extra_context=None):
        self.form = self.orig_form
        self.prepopulated_fields = {"slug": ("name",)}
        self.exclude = ('images', )
        return super(CarAdmin, self).add_view(request)
class CategoryAdmin(admin.ModelAdmin):
    list_display = ['title', 'description']
admin.site.register(Car, CarAdmin)
admin.site.register(Category, CategoryAdmin)