Ficus (figs) and their agaonid wasp pollinators present an ecologically important mutualism that also provides a rich comparative system for studying functional co-diversification throughout its coevolutionary history (similar to 75 million years). We obtained entire nuclear, mitochondrial, and chloroplast genomes for 15 species representing all major clades of Ficus. Multiple analyses of these genomic data suggest that hybridization events have occurred throughout Ficus evolutionary history. Furthermore, cophylogenetic reconciliation analyses detect significant incongruence among all nuclear, chloroplast, and mitochondrial-based phylogenies, none of which correspond with any published phylogenies of the associated pollinator wasps. These findings are most consistent with frequent host-switching by the pollinators, leading to fig hybridization, even between distantly related clades. Here, we suggest that these pollinator host-switches and fig hybridization events are a dominant feature of fig/wasp coevolutionary history, and by generating novel genomic combinations in the figs have likely contributed to the remarkable diversity exhibited by this mutualism. Figs and their wasp pollinators are a classic example of coevolution. By assembling and analysing genomes from across the Ficus clade, authors suggest that fig hybridization driven by pollinator host-switching in this obligate pollination system, is more common than previously thought.