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Symbiotic relationships shape the evolution of organisms. Fungi in the genus Escovopsis share an evolutionary history with the fungus-growing “attine” ant system and are only found in association with these social insects. Despite this close relationship, there are key aspects of Escovopsis evolution that remain poorly understood. To gain further insight into the evolutionary history of these unique fungi, we delve deeper into Escovopsis’ origin and distribution, considering the largest sampling, so far, across the Americas. Furthermore, we investigate Escovopsis’ trait evolution, and relationship with attine ants. We demonstrate that, while the genus originated approximately 56.9 Mya, it only became associated with 'higher attine' ants in the last 38 My. Our results, however, indicate that it is likely that the ancestor of Escovopsis lived in symbiosis with early-diverging fungus-growing ants. Since then, the fungi have evolved morphological and physiological adaptations that have increased their reproductive efficiency, possibly to overcome barriers mounted by the ants and their other associated microbes. Taken together, these results provide new clues as to how Escovopsis has evolved within the context of this complex symbiosis and shed light on the evolutionary history of the fungus-growing ant system.