Sexual dimorphism is a major component of morphological variation across the tree of life, but the mechanisms underlying phenotypic differences between sexes of a single species are poorly understood. We examined the population genomics and biogeography of the common palmflyElymnias hypermnestra, a dual mimic in which female wing colour patterns are either dark brown (melanic) or bright orange, mimicking toxicEuploeaandDanausspecies, respectively. As males always have a melanic wing colour pattern, this makesE. hypermnestraa fascinating model organism in which populations vary in sexual dimorphism. Population structure analysis revealed that there were three genetically distinctE. hypermnestrapopulations, which we further validated by creating a phylogenomic species tree and inferring historical barriers to gene flow. This species tree demonstrated that multiple lineages with orange females do not form a monophyletic group, and the same is true of clades with melanic females. We identified two single nucleotide polymorphisms (SNPs) near the colour patterning geneWntAthat were significantly associated with the female colour pattern polymorphism, suggesting that this gene affects sexual dimorphism. GivenWntA's role in colour patterning across Nymphalidae,E. hypermnestrafemales demonstrate the repeatability of the evolution of sexual dimorphism.