Speciation in pollinating seed predators such as fig wasps (Hymenoptera: Agaonidae) is likely to have been influenced by a combination of ecological and geographical isolating mechanisms, but recent molecular analyses of fig wasps have focused on pollinator specialization as the main factor driving speciation. This study investigates the contribution of geographic modes of speciation such as dispersal, vicariance, and isolation by distance. We sampled haplotypes of mitochondrial cytochrome oxidase I from Ceratosolen pollinators of six geographically widespread Australasian fig (Moraceae: Ficus) species, including four species spanning Wallacea. Phylogenetic analysis investigated the extent of host conservatism and host switching accompanying divergence in Ceratosolen. Geographically widespread Ceratosolen showed deep intraspecific divergence exceeding or comparable to divergence between named sister species. Maximum parsimony and Bayesian analyses supported species monophyly in five of six cases, whereas results for a sixth species were equivocal. Bayesian divergence time estimation suggested dispersal across Wallacea during the Miocene epoch, after the collision of Australian and Asian continental plates. Cryptic species were evident in all six focal taxa. Because the deep mitochondrial divergence within these taxa is regionally distributed, allopatric divergence provides a simple explanation for the existence of these cryptic lineages pollinating widespread fig species. We found little evidence of divergence accompanied by host switching. The ancient origin of cryptic and geographically isolated species suggests that long-distance dispersal may be rare in Ceratosolen and that host associations are generally conserved during range expansion.