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Abstract Understanding how and when key novel adaptations evolved is a central goal of evolutionary biology. Within theimmigrans‐tripunctataradiation ofDrosophila, many mushroom‐feeding species are tolerant of host toxins, such as cyclopeptides, that are lethal to nearly all other eukaryotes. In this study, we used phylogenetic and functional approaches to investigate the evolution of cyclopeptide tolerance in theimmigrans‐tripunctataradiation ofDrosophila. First, we inferred the evolutionary relationships among 48 species in this radiation using 978 single copy orthologs. Our results resolved previous incongruities within species groups across the phylogeny. Second, we expanded on previous studies of toxin tolerance by assaying 16 of these species for tolerance to α‐amanitin and found that six of them could develop on diet with toxin. Finally, we asked how α‐amanitin tolerance might have evolved across theimmigrans‐tripunctataradiation, and inferred that toxin tolerance was ancestral in mushroom‐feedingDrosophilaand subsequently lost multiple times. Our findings expand our understanding of toxin tolerance across theimmigrans‐tripunctataradiation and emphasize the uniqueness of toxin tolerance in this adaptive radiation and the complexity of biochemical adaptations.