In butterflies, wing colour pattern diversity and scale types are controlled by a few genes of large effect that regulate colour pattern switches between morphs and species across a large mimetic radiation. One of these genes, , has been repeatedly associated with colour pattern evolution in butterflies. Here we carried out CRISPR knockouts in multiple species and show that is a major determinant of scale cell identity. Chromatin accessibility profiling and introgression scans identified -regulatory regions associated with discrete phenotypic switches. CRISPR perturbation of these regions in black hindwing genotypes recreated a yellow bar, revealing their spatially limited activity. In the lineage, the candidate CRE from yellow-barred phenotype morphs is interrupted by a transposable element, suggesting that -regulatory structural variation underlies these mimetic adaptations. Our work shows that functionally controls scale colour fate and that its -regulatory regions control a phenotypic switch in a modular and pattern-specific fashion.