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Abstract The Rufous-collared Sparrow (Zonotrichia capensis) shows phenotypic variation throughout its distribution. In particular, the Patagonian subspecies Z. c. australis is strikingly distinct from all other subspecies, lacking the black crown stripes that characterize the species, with a uniformly grey head and overall paler plumage. We sequenced whole genomes of 18 individuals (9 Z. c. australis and 9 from other subspecies from northern Argentina) to explore the genomic basis of these color 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 suppression of tumorigenicity 5 (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 or against gene flow on populations in physical and genetic contact. Mitochondrial DNA indicated that Z. c. australis diverged from other subspecies ~400,000 years ago, suggesting a putative role of Pleistocene glaciations. Phenotypic differences are consistent with Gloger’s rule, which predicts lighter-colored individuals in colder and drier climates like that of Patagonia.