Understanding the genetic basis of local adaptation and the distribution of standing genetic variation is imperative for biodiversity conservation as species decline globally. The Atlantic song sparrow (Melospiza melodia atlantica) is a specialist subspecies of conservation concern that is adapted to the coastal habitats of eastern North America and interbreeds with a widespread, parapatric generalist subspecies, the eastern song sparrow (M. m. melodia). Because the Atlantic and eastern song sparrows offer an ideal opportunity to explore the evolutionary dynamics of local adaptation with gene flow, we examined the genomic architecture of divergence and the basis of coastal adaptation using whole-genome sequencing of these subspecies. We identified a polygenic basis for coastal adaptation, with candidate genes related to osmoregulation, plumage pigmentation, and bill size. Divergent genes were dispersed throughout a homogenous genomic background, demonstrating that strong natural selection is the key force maintaining differentiation between these subspecies despite gene flow. Notably, some candidate genes were located near centromeres and telomeres, suggesting regions of suppressed recombination may play some role in the maintenance of local adaptation despite gene flow in this system. We found population structure within the Atlantic song sparrow, with southern barrier islands making a up a key portion of the range of this subspecies and each island comprising a distinct gene cluster, which may inform future conservation management decisions. This system emphasizes the need for high-resolution genomic data to characterize the basis of adaptive differentiation and inform effective conservation strategies for systems with extensive gene flow.