The Rufous-collared Sparrow (Zonotrichia capensis) shows phenotypic and behavioural variation throughout its continental distribution. In particular, the Patagonian subspecies Z. c. australis is strikingly distinct from other subspecies, lacking the black crown stripes that characterize the species, with a uniformly grey head or one with only subtle traces of black, and overall paler plumage. We sequenced whole genomes of 18 individuals (nine Z. c. australis and nine from other subspecies from northern Argentina) to explore the genomic basis of these colour differences and to investigate how they may have evolved. We detected a single ~465-kb divergence peak on chromosome 5 that contrasted with a background of low genomic differentiation and contains the ST5 gene. ST5 regulates RAB9A, which is required for melanosome biogenesis and melanocyte pigmentation in mammals, making it a strong candidate gene for the melanic plumage polymorphism within Z. capensis. This genomic island of differentiation may have emerged because of selection acting on allopatric populations. Concordantly, mitochondrial DNA indicated that Z. c. australis diverged from other subspecies ~400,000 years ago, probably as a consequence of Pleistocene glaciations. Phenotypic differences are consistent with Gloger’s rule, which predicts lighter coloured individuals in colder and drier climates like that of Patagonia. Future studies should focus on a contact zone in northern Patagonia where individuals show intermediate colour patterning, most likely as a result of gene flow between subspecies, to test whether colour differences are promoting the early speciation of Z. c. australis through assortative mating.