Animals have evolved a vast array of colors and color patterns in response to natural, sexual, and artificial selection. Domestic rock pigeons (Columba livia) are a stunning example of this diversity because different individuals within the same species vary tremendously in color and color pattern. Classical genetics suggest that four alternative alleles (T-check, Checker, Bar, Barless in decreasing order of dominance and melanism) at a single locus determine wing color pattern. Although the Bar pattern is thought to be the ancestral phenotype, birds with the Checker and T-check patterns are more numerous in urban environments, possibly due to enhanced fitness. In this study we investigate the genetic basis of wing color pattern variation. We performed whole-genome comparisons between Bar and Checker birds to identify a candidate region containing just a few genes that was highly differentiated between the two phenotypes. Surprisingly, cross-species sequence comparisons suggest that a haplotype in this region that is shared by all Checker birds was introgressed into the rock pigeon from a different species, providing a striking example of cross-species transmission of a potentially adaptive phenotype. One gene in the candidate region shows expression differences among Bar, Checker, and T-check alleles in regenerating feathers indicating a cis-regulatory change at this locus. Lastly, we find that Barless birds, which have an increased incidence of vision defects, are homozygous for a nonsense mutation in a gene that is associated with blindness in humans. Remarkably, the same mutation we find in pigeons is also observed in two human families with hereditary blindness. This study highlights unexpected molecular links between color pattern, adaptive introgression, and vision defects in a classical model organism.