The fungus-growing ants have long provided a spectacular example of co-evolutionary integration between distantly related taxa. Their ecological success is thought to depend largely on the evolutionary alignment of reproductive interests between ants and fungi following vertical co-transmission of the symbiont genotypes, aided by the ancient suppression of fungal sexual reproduction. We will show that the association between ant lineages and cultivar genotypes is a diffuse one, where genetic associations are obliterated by frequent host shifts and where cultivars can exist as large panmictic populations linked by long-distance cultivar dispersal, likely using spores.We first provide evidence for recombination in attine cultivars, based on conservation of meiosis-specific genes, the existence of recombination between nuclear loci and direct observations of recombination in an isolated invasive population of a leaf-cutting ant. Using microsatellite markers, we show that cultivar fungi associated with five sympatric leaf-cutting ant species have little population structuring with respect host ant genotype, suggesting that cultivar exchange dwarfs selective forces acting to create co-adaptive ant-cultivar combinations.  Then, we show that populations of the ant Trachymyrmex septentrionalis have undergone extensive sharing of cultivar lineages, probably representing different fungal species. Finally, we document extensive long-distance horizontal transmission of fungal genes between leaf-cutter taxa resident on the mainland and those endemic to Cuba, suggesting both lack of specificity in ant/cultivar co-evolutionary interactions and independent long-range dispersal by the cultivar. We conclude by discussing the implications of co-evolutionary diffuseness, highlighting the possibility that asymmetrical species boundaries, such as the many-to-one interaction between the leaf-cutting ants and their dominant cultivar fungus, play an important role in adaptive co-evolution in this system. The observation of prevalent diffuse co-evolution in the attine ant-fungus symbiosis parallels recent discoveries in other systems, suggesting that one-to-one specificity in mutualistic interactions is evidently not common, as once thought.