Every CHERUB agent is assigned to an adult handler.

Handlers help to develop the individual curriculum that each pupil on campus follows. They liase with the Mission Controllers, helping to make decisions about what agents are suitable for particular operations.

Most importantly, a CHERUB handler takes on the role of a surrogate parent, dealing with the disciplinary and emotional needs of the cherubs.

The handler is also responsible for setting up an agent's post CHERUB identity.

All handlers also have a teaching or coaching role on campus.