Across most of the range of the fungus-growing ant Mycocepurus smithii, queens reproduce asexually, males are absent, and workers are sterile. The clonal ants depend on gardens of clonal fungi for food, yet M.smithii has the most extensive distribution (Argentina-Mexico) and highest population densities of any fungus-growing ant. Sexual populations exist in the Amazon basin; these appear to be the source of independently evolved asexual lineages. Phylogenetic analyses indicate that M.smithii originated 0.5–1.65 million years ago and is monophyletic, making a hybrid origin of asexuality unlikely. AMOVA and ParaFit analyses of ant microsatellite-genotypes and corresponding fungal ITS-types implicate either frequent cultivar exchange between ant lineages or frequent de-novo domestication of fungi from feral populations. Cultivar switching may be a strategy to purge cultivars that are locally mal-adapted or that accumulated deleterious mutations (Muller’s ratchet) under long-term asexuality. Rather than partner-fidelity feedback under strict vertical cultivar transmission, symbiont choice by ants and local adaptations of ant-fungus combinations may play an important role in the coevolution between M. smithii and its fungal symbionts.