Understanding genetic structure and diversity within species can uncover associations with environmental and geographic attributes that highlight adaptive potential and inform conservation and management. The California gnatcatcher, Polioptila californica, is a small songbird found in desert and coastal scrub habitats from the southern end of Baja California Sur to Ventura County, California. Lack of congruence among morphological subspecies hypotheses and lack of measurable genetic structure found in a few genetic markers led to questions about the validity of subspecies within P. californica and the listing status of the coastal California gnatcatcher, P. c. californica. As a U.S. federally threatened subspecies, P. c. californica is recognized as a flagship for coastal sage scrub conservation throughout southern California. We used restriction site-associated DNA sequencing to develop a genomic dataset for the California gnatcatcher. We sampled throughout the species' range, examined genetic structure, gene–environment associations, and demographic history, and tested for concordance between genetic structure and morphological subspecies groups. Our data support two distinct genetic groups with evidence of restricted movement and gene flow near the U.S.- Mexico international border. We found that climate-associated outlier loci were more strongly differentiated than climate neutral loci, suggesting that local climate adaptation may have helped to drive differentiation after Holocene range expansions. Patterns of habitat loss and fragmentation are also concordant with genetic substructure throughout the southern California portion of the range. Finally, our genetic data supported the morphologically defined P. c. californica as a distinct group, but there was little evidence of genetic differentiation among other previously hypothesized subspecies in Baja California. Our data suggest that retaining and restoring connectivity, and protecting populations, particularly at the northern range edge, could help preserve existing adaptive potential to allow for future range expansion and long-term persistence of the California gnatcatcher.