The associations between figs and their mutualistic and parasitic wasps have been extensively studied and provide textbook examples of coevolution, extreme ecological specialization, and parallel speciation. The paradigm that figs and their pollinator and parasitic wasps exhibit a one-to-one species relationship across all 750-plus Ficus spp. is both ecologically and evolutionarily appealing. With few exceptions, this paradigm has held true for both morphological and genetic studies. The studies described in this thesis tested this assumption of species-specificity and examined the fine scale patterns of differentiation within the fig-fig wasp system by studying intraspecific evolutionary concordance between the Sonoran Desert rock fig, F. petiolaris, and an associated non-pollinating wasp, the floral parasite, Idarnes. With our detailed analysis between the rock fig and its parasites, we were able to identify an apparent example of relaxed coevolutionary relationships, with evidence of four morphologically and genetically independent wasp lineages attacking a single host species. Placed in a broader phylogenetic context, these multiple wasp lineages on a single host species appeared to be the result of relatively recent host shifts and possibly in situ diversification on F. petiolaris. Further, a sampling of Idarnes spp. from across New World Urostigma hosts also revealed evidence of multiple lineages coexisting on the same host species, suggesting that host-shifts and other processes acting counter to the one-wasp-one-host species relationship may be relatively common. In contrast, at a finer phylogeographic scale we found evidence for concordant patterns of genetic structure between the rock fig and one of its parasite lineages, suggesting the possibility of coevolutionary relationships below the species level. Together, these results indicate that the coevolutionary relationships between the rock fig and its Idarnes floral parasites are complex and do not conform to a simple model of one-to-one species specificity and strict cospeciation. These unanticipated results beg for further detailed evolutionary and ecological examinations at all taxonomic scales of this diverse and highly complex model system. Such studies hold the promise of improving our understanding of coevolutionary interactions in a wide variety of host-parasite and mutualistic systems.