Figs and their pollinating wasps are perhaps the classic example of an obligate mutualism. In addition, figs have a suite of non-pollinating parasitic wasps whose basic ecology is largely undescribed. Figs therefore present the interesting situation of a host that has two closely related taxa associated with it, one of which is mutualistic, the other parasitic. We show that the wasps belonging to the most abundant genus of New World parasites, the Idarnes wasps, develop at the expense of the pollinating wasps and not the viable seeds. However, the Idarnes wasps are not true parasitoids. We interpret these results to mean that the Idarnes wasps are in direct competition with the pollinator wasps for the same pool of flowers in which the larvae of either group can develop. Further, we infer that there is also a pool of flowers that cannot be exploited by either of these taxa. The observation that the pollinators and the parasites oviposit from different sides of the fruit strongly suggests that the basis for preserving some of the flowers to develop as viable seeds is not a direct result of spatial position of the ovaries or style length, as has been previously suggested. This idea is corroborated by detailed observations in many other fig systems. Taken together, these findings suggest an explanation for the stability of the fig-fig-pollinating wasp mutualism, as well as the structure of its parasite community.