Animals that cooperate with nonrelatives represent a challenge to inclusive fitness theory, unless cooperative behavior is shown to provide direct fitness benefits. Inheritance of breeding resources could provide such benefits, but this route to cooperation has been little investigated in the social insects. We show that nest inheritance can explain the presence of unrelated helpers in a classic social insect model, the primitively eusocial wasp Polistes dominulus. We found that subordinate helpers produced more direct offspring than lone breeders, some while still subordinate but most after inheriting the dominant position. Thus, while indirect fitness obtained through helping relatives has been the dominant paradigm for understanding eusociality in insects, direct fitness is vital to explain cooperation in P. dominulus.