The build‐up of the phenotypic differences that distinguish species has long intrigued biologists. These differences are often inherited as stable polymorphisms that allow the cosegregation of adaptive variation within species, and facilitate the differentiation of complex phenotypes between species. It has been suggested that the clustering of adaptive loci could facilitate this process, but evidence is still scarce. Here, we used QTL analysis to study the genetic basis of phenotypic differentiation between coastal populations of the Australian wildflower Senecio lautus. We found that a genomic region consistently governs variation in several of the traits that distinguish these contrasting forms. Additionally, some of the taxon‐specific traits controlled by this QTL cluster have evolved repeatedly during the adaptation to the same habitats, suggesting that it could mediate divergence between locally adapted forms. This cluster contains footprints of divergent natural selection across the range of S. lautus, which suggests that it could have been instrumental for the rapid diversification of this species.