SummaryIdentifying the genes and mutations that drive phenotypic variation and which are subject to selection is crucial for understanding evolutionary processes. Mormon Fritillary butterflies (Speyeria mormonia) exhibit a striking wing color polymorphism throughout their range: typical morphs bear silver spots on their ventral surfaces, and can co-occur with unsilvered morphs displaying a dull coloration1. Through genome-wide association studies in two polymorphic populations, we fine-map this difference in silvering to the 3’ region of the transcription factor geneoptix. The expression ofoptixis confined to the unsilvered regions that surround the spots, and these patterns are transformed to a silver identity uponoptixRNAi knockdown, implicatingoptixas a repressor of silver scales in this butterfly. We show that the unsilveredoptixhaplotype shows signatures of recent selective sweeps, and that this allele is shared with the monomorphic, unsilvered speciesSpeyeria hydaspe, suggesting that introgressions facilitate the exchange of variants of adaptive potential across species. Remarkably, these findings parallel the role of introgressions andcis-regulatory modulation ofoptixin shaping the aposematic red patterns ofHeliconiusbutterflies2–7, a lineage that separated fromSpeyeria45 million years ago8. The genetic basis of adaptive variation can thus be more predictable than often presumed, even for traits that appear divergent across large evolutionary distances.Graphical Abstract