Numerous studies have tested for geographically congruent spatial genetic structures and population units in codistributed species. Yet, few have elucidated the relative importance of biogeographic influences versus ecological interactions in determining the congruence of genetic structure in coevolving species. Here, we present the first study testing for genetic codifferentiation in a widely distributed and highly-coevolved mutualism, in which symbiont gene dispersal is expected to be positively correlated. In the fig, Ficus petiolaris, and its host-specific Pegoscapus pollinating wasp, we evaluated the extent to which geographical patterns of differentiation in each species are similar and explained by shared sources of vicariance, co-dispersal, or species-dependent factors. In both species, the Trans-Mexican Volcanic Belt was a major source of vicariance differentiating southern and northern phylogroups. Within these phylogroups, however, fig and pollinator showed surprisingly different population genetic structure. In F. petiolaris, the Gulf of California was a strong phylogeographic break in the northern phylogroup. In contrast, within its northern phylogroup, Pegoscapus sp. showed no genetic structure and only weak isolation by distance over a 1500 km range. In the southern phylogroup, exceptional genetic differentiation was observed among populations separated by as little as 300 km. Despite mutual selective pressure between figs and fig wasps, and the role of fig wasps in fig gene flow, we conclude that range-wide patterns of genetic differentiation are primarily influenced by biological features unique to each species rather than by shared sources of vicariance or correlated gene dispersal.