The distribution of genetic and phenotypic variation in both hosts and parasites over their geographic ranges shapes coevolutionary dynamics. Specifically, concordant host and parasite distributions facilitate localized adaptation and further specialization of parasite genotypes on particular host genotypes. We here compare genetic population structure of the cultivated fungi of the fungus-growing ant Apterostigma dentigerum and of the cultivar-attacking fungus, Escovopsis, to determine whether these microbial associations have evolved or are likely to evolve genotype-genotype specialization. Analyses based on amplified fragment length polymorphism (AFLP) genotyping of host cultivars and pathogenic Escovopsis from 77 A. dentigerum colonies reveal that populations of hosts and pathogens are not similarly diverged and that host and pathogen genetic distances are uncorrelated, indicating that genetically similar parasites are not infecting genetically similar hosts. Microbial bioassays between pathogens and cultivars of different genotypes and from different populations show little pairwise specificity; most Escovopsis strains tested can successfully infect all cultivar strains with which they are paired. These molecular and experimental data suggest that Escovopsis genotypes are not tightly tracking cultivar genotypes within the A. dentigerum system. The diffuse nature of this host-pathogen association, in which pathogen genotypes are not interacting with a single host genotype but instead with many different hosts, will influence evolutionary and ecological disease dynamics of the fungus-growing ant-microbe symbiosis.