Understanding why individuals within altruistic societies forego reproduction to raise others' offspring has fascinated scientists since Darwin. Although worker polymorphism is thought to have evolved only in sterile workers, worker subcastes appear to be common among social invertebrates and vertebrates. We asked whether sterility accompanies eusociality and morphological differentiation in snapping shrimps (Synalpheus) - the only known marine eusocial group. We show that workers in S. elizabethae are reproductively totipotent, and that female — but not male — gonadal development and mating are mediated by the presence of a queen, apparently without physical aggression. In queenless experimental colonies, a single immature female worker typically became ovigerous, and no female workers matured in colonies with a resident queen. Thus, eusocial shrimp workers retain reproductive totipotency despite signs of morphological specialization. The failure of most female workers to mature is instead facultative and mediated by the presence of the queen, ensuring her reproductive monopoly.