Habitat loss, flood control infrastructure, and drought have left most of southern California and northern Baja California’s native freshwater fish fauna on the brink of extinction, including the endangered unarmored threespine stickleback (Gasterosteus aculeatus williamsoni). This subspecies, an unusual morph lacking the typical lateral bony plates of the G. aculeatus complex, occurs at arid southern latitudes in the eastern Pacific Ocean and survives in only three inland locations. Managers have been stymied by a lack of molecular data to prioritize conservation efforts, including basic questions about the ancestry and genetic distinctiveness of unarmored populations. We sampled G. aculeatus from 36 localities and used microsatellites and whole genome data to place unarmored populations within the broader evolutionary context of G. aculeatus across southern California/northern Baja California. We identified three genetic groups, with none consisting solely of unarmored populations. Unlike G. aculeatus at northern latitudes, where Pleistocene glaciation has produced similar historical demographic profiles across populations, we found markedly different demographies depending on sampling location, with inland unarmored populations tending to show steeper declines and lower heterozygosity compared to low armored populations in coastal lagoons. One exception involved the only high-elevation population in the region, where the demography and alleles of unarmored fish were similar to low-armored populations near the coast, exposing one of several cases of artificial translocation. Our results suggest that the current ‘management-by-phenotype’ approach is incidentally protecting the most imperiled populations; however, redirecting efforts toward the evolutionary units, regardless of phenotype, may be more effective at preserving adaptive potential.