Figs and their associated mutualistic and parasitic wasps have been a focus of intensive ecological and evolutionary research due to their diversity, unusual reproductive biology, and highly coevolved interspecific relationships. Due to the ecological dependence of their interactions, fig wasps were once considered to be fig-species specific and to cospeciate with their hosts, however, a growing body of evidence reveals mixed support for species specificity and the importance of additional evolutionary processes (e.g., host switching) structuring these long-term interactions. Our research on the genus Idarnes Walker, 1843 (Hymenoptera, Agaonidae), a common non-pollinating wasp of New World fig flowers, reveals a community in which multiple wasp species coexist on the same host in space and time. Using both molecular and morphological data, we identify five distinct Idarnes lineages associated with a single host fig species, Ficus petiolaris Kunth, 1817 (Rosales, Moraceae). A comprehensive phylogenetic analysis including Idarnes species from numerous host fig species reveals that the lineages associated with F. petiolaris do not form a monophyletic group but are distantly related, suggesting multiple independent colonization events and subsequent diversification. Morphological and ecological data provide support that the wasps are partitioning niches within the figs, explaining the coexistence of these diverse lineages on the same host fig.These results, coupled with a growing body of research on pollinating and non-pollinating fig wasps, bring into focus a more dynamic picture of fig and fig wasp coevolution and highlight how wasp lineage divergence and niche partitioning contributes to increased species diversity and community structure on a single fig host.