No user.home_folder or user.trash_folder

models.py

class User(Base):
    __tablename__ = 'users'

    id = Column(Integer, primary_key=True)
    name = Column(String(80), unique=True)

    home_folder_id = Column(Integer, ForeignKey("folders.id"))
    home_folder = relationship("Folder",
                               foreign_keys="User.home_folder_id",
                               backref="home_user")

    trash_folder_id = Column(Integer, ForeignKey("folders.id"))
    trash_folder = relationship("Folder",
                                foreign_keys="User.trash_folder_id",
                                backref="trash_user")

class Entry(Base):
    __tablename__ = 'entries'

    id = Column(Integer, primary_key=True)
    name = Column(String(80), unique=True)
    type = Column(String(50))

    __mapper_args__ = {
        'polymorphic_identity': classmethod.__class__.__name__,
        'polymorphic_on': type,
        'with_polymorphic': '*'
    }


class Folder(Entry):

    # Enum Folder types
    # TODO: Could be a good idea to transform these enums into Classes. So they can have different behaviors if needed
    class FolderType(enum.Enum):
        home = 'home'
        trash = 'trash'
        folder = 'folder'

    __tablename__ = 'folders'

    # TODO: Instead of using a string 'entry.id', can we use Entry.id?
    id = Column(Integer, ForeignKey('entries.id'), primary_key=True)

    folder_type = Column(Enum(FolderType))
    description = Column(Text)

    entries = relationship("Entry",
                           secondary=folder_entry_association_table,
                           backref=__tablename__)

    creator_id = Column(Integer, ForeignKey("users.id"))

    creator = relationship("User",
                           foreign_keys="Folder.creator_id",
                           backref=__tablename__)

    __mapper_args__ = {
        'polymorphic_identity': "Folder"
    }

Test_user.py

new_user = User(name=name)

home_folder = Folder(name="Home",
                     folder_type=Folder.FolderType.home,
                     creator=new_user)

trash_folder = Folder(name="Trash",
                      folder_type=Folder.FolderType.trash,
                      creator=new_user)

session.add(home_folder)
session.add(trash_folder)
session.add(new_user)
session.commit()

## home_folder and trash_folder are ok.
## new_user.home_folder => Nothing, new_user.trash_folder => Nothing

The problem is you have two different foreign keys. You're setting the creator relationship, which sets the creator_id foreign key. But sqlalchemy has no idea this is supposed to also set new_user.home_folder or new_user.trash_folder, because those use different foreign keys.