By mechanisms that are still unknown, gall wasps (Cynipidae) induce plants to form complex galls, inside which their larvae develop. The family also includes inquilines (phytophagous forms that live inside the galls of other gall inducers) and possibly also parasitoids of gall inducers. The origin of cynipids is shrouded in mystery, but it has been clear for some time that a key group in making progress on this question is the ‘figitoid inquilines’. They are gall-associated relatives of cynipids, whose biology is poorly known. Here, we report the first detailed data on the life history of a figitoid inquiline, the genus Parnips. Dissections of mature galls show that Parnips nigripes is a parasitoid of Barbotinia oraniensis, a cynipid that induces single-chambered galls inside the seed capsules of annual poppies (Papaver rhoeas and P. dubium). Galls with pupae of Parnips nigripes always contain the remains of a terminal-instar larva of B. oraniensis. The mandibles of the terminal-instar larva of P. nigripes are small and equipped with a single sharp tooth, a shape that is characteristic of carnivorous larvae. The weight of P. nigripes pupae closely match that of the same sex of B. oraniensis pupae, indicating that Parnips makes efficient use of its host and suggesting that ovipositing Parnips females lay eggs that match the sex of the host larva. Dissection of young galls show that another species of Parnips, hitherto undescribed, spends its late larval life as an ectoparasitoid of Iraella hispanica, a cynipid that induces galls in flowers of annual poppies. These and other observations suggest that Parnips shares the early endoparasitic-late ectoparasitic life history described for all other cynipoid parasitoids. Our findings imply that gall wasps evolved from parasitoids of gall insects. The original hosts could not have been cynipids but possibly chalcidoids, which appear to be the hosts of several extant figitoid inquilines. It is still unclear whether the gall inducers evolved rapidly from these ancestral parasitoids, or whether they were preceded by a long series of intermediate forms that were phytophagous inquilines.