The emergence of queens and workers from solitary antecedents mark a major evolutionary transition in the history of life. The solitary progressive provisioning wasp Synagris cornuta, a member of the subfamily basal to eusocial vespid wasps (Eumeninae), alternates between behavioral states characterized as queen-like and worker-like. Akin to a queen in eusocial wasps, a S. cornuta female initiates construction of a cell into which she oviposits, and then, similar to a worker, she cares for the brood as it develops. The Ovarian Groundplan (OGP) hypothesis for caste origins predicts that these behavioral states are associated with cyclical changes in ovarian status, where females performing queen-like tasks have eggs and those performing worker-like tasks possess only small oocytes. Our findings show strong support for the OGP hypothesis: the ovaries of S. cornuta females undergo differential oogenesis depending on the behavioral phase: the largest oocyte in the ovaries of females building a cell progress faster compared to that of females attending brood. Yet contrary to the OGP hypothesis, neither juvenile hormone nor ecdysteroids are associated with the reproductive cycle. Finally, the cuticular hydrocarbon profile showed no link with ovarian status, suggesting that fertility signals evolved subsequent to the emergence of group living.