Mutualisms are interactions between two species in which the fitnesses of both symbionts benefit from the relationship. Although examples of mutualism are ubiquitous in nature, the ecology, evolution, and stability of mutualism has rarely been studied in the broader, multispecies community context in which they occur. The pollination mutualism between figs and fig wasps provides an excellent model system for investigating interactions between obligate mutualists and antagonists. Compared to the community of non-pollinating fig wasps that develop within figs inflorescences at the expense of fig seeds and pollinators, consequences of interactions between female pollinating wasps and their host-specialist nematode parasites is much less well understood. Here we focus on a tri-partite system comprised of a fig (Ficus petiolaris), pollinating wasp (Pegoscapus sp.), and nematode (Parasitodiplogaster sp.), investigating geographical variation in the incidence of attack and mechanisms through which nematodes may limit the fitness of their wasp hosts at successive life history stages. Observational data reveals that nematodes are ubiquitous across their host range in Baja California, Mexico; that the incidence of nematode infection varies across seasons within- and between locations, and that infected pollinators are sometimes associated with fitness declines through reduced offspring production. We find that moderate levels of infection (1-9 juvenile nematodes per host) are well tolerated by pollinator wasps whereas higher infection levels (≥10 nematodes per host) are correlated with a significant reduction in wasp lifespan and dispersal success. This overexploitation, however, is estimated to occur in only 2.8% of wasps in each generation. The result that nematode infection appears to be largely benign – and the unexpected finding that nematodes frequently infect non-pollinating wasps – highlight gaps in our knowledge of pollinator-Parasitodiplogaster interactions and suggest previously unappreciated ways in which this nematode may influence fig and pollinator fitness, mutualism persistence, and non-pollinator community dynamics.