<p>Grasshopper sparrows (<i>Ammodramus savannarum</i>) face significant conservation challenges with some populations, such as the non-migratory group in central Florida (<i>A. s. floridanus</i>), being federally listed as endangered in the United States. To assess their genomic distinction and differentiation, we conducted a genome-wide assessment of grasshopper sparrows representing migratory and non-migratory populations that breed within the continental United States. Based on reference-aligned single nucleotide polymorphisms (SNPs), we could not identify genetic structure that associated sub-specific taxonomy to evolutionary divergence. We used coalescent modeling to evaluate the demographic history and test competing hypotheses about degrees of reproductive isolation. Stairway plot analyses revealed a steep decline in the effective population sizes of the eastern subspecies over the past millennium. Coalescent model testing supported a demographic history of decline and reproductive isolation following the divergence between migratory and non-migratory populations, with evidence of asymmetric gene flow from migratory sparrows into <i>A. s. floridanus</i> in the last century<i>.</i> Our results support the consideration of North American breeding populations of grasshopper sparrows as recently diverged lineages with evidence of contemporary gene flow between recognized eastern lineages.</p>