Despite recent progress, we still know relatively little about the genetic architecture that underlies adaptation to divergent environments. Determining whether the genetic architecture of phenotypic adaptation follows any predictable patterns requires data from a wide variety of species. However, in many organisms, genetic studies are hindered by the inability to perform genetic crosses in the laboratory or by long generation times. Admixture mapping is an approach that circumvents these issues by taking advantage of hybridization that occurs between populations or species in the wild. Here, we demonstrate the utility of admixture mapping in a naturally occurring hybrid population of threespine sticklebacks (Gasterosteus aculeatus) from Enos Lake, British Columbia. Until recently, this lake contained two species of sticklebacks adapted to divergent habitats within the lake. This benthic–limnetic species pair diverged in a number of phenotypes, including male nuptial coloration and body shape, which were previously shown to contribute to reproductive isolation between them. However, recent ecological disturbance has contributed to extensive hybridization between the species, and there is now a single, admixed population within Enos Lake. We collected over 500 males from Enos Lake and found that most had intermediate nuptial colour and body shape. By genotyping males with nuptial colour at the two extremes of the phenotypic distribution, we identified seven genomic regions on three chromosomes associated with divergence in male nuptial colour. These genomic regions are also associated with variation in body shape, suggesting that tight linkage and/or pleiotropy facilitated adaptation to divergent environments in benthic–limnetic species pairs.