Next-generation sequencing technologies are increasingly being employed to explore patterns of genomic variation in avian taxa previously characterized using morphology and/or traditional genetic markers. The hybridization dynamics of the Northern Flicker complex have received considerable attention, primarily due to the conspicuous plumage differences among these birds and the geographically extensive hybrid zone between the Red-shafted (Colaptes auratus cafer) and Yellow-shafted (Colaptes auratus auratus) flickers in the Great Plains region of North America. However, no traditional molecular techniques have been able to differentiate these 2 morphologically well-defined taxa from one another, or conclusively from the closely related Gilded Flicker (Colaptes chrysoides). Here, we use a next-generation sequencing approach to assess the genetic diversity and evolutionary history of these 3 taxa. We confirm the overall low levels of differentiation found using traditional molecular markers, but are able to distinguish between the 3 taxa for the first time, using a dataset of thousands of SNP loci distributed across the genome. Through demographic modeling and phylogenetic reconstructions, we find that Red-shafted and Yellow-shafted flickers are likely sister taxa, and that their divergence from the Gilded Flicker was comparatively older. The low level of divergence and lack of fixed differences in our dataset between Red-shafted and Yellow-shafted flickers, in particular, suggests whole-genome re-sequencing may be necessary to assess the dynamics of their hybridization and identify the genetic basis of their striking differences in plumage.