Pygmy rabbits (Brachylagus idahoensis) are closely associated with sagebrush steppe habitat across the western United States, and loss and fragmentation of this habitat has contributed to the near extirpation of the Columbia Basin population in Washington state. The Columbia Basin (WA-CB) pygmy rabbit was listed under the Endangered Species Act in 2003, and recovery efforts have included captive breeding, reintroduction, and genetic rescue with translocation of rabbits from populations across the species range. We used restriction site-associated DNA sequencing (RADseq) to determine population genetic structure across the pygmy rabbit range, test for genomic signatures of adaptive divergence among populations, assess the genetic distinctiveness of the ancestral WA-CB population, and identify loci useful for monitoring ancestry in the current admixed WA-CB population. Our dataset included 9,794 single nucleotide polymorphisms (SNPs) across 123 individuals. We identified four distinct genetic groups: (1) WA-CB, (2) Great Basin (3) northern Utah/Wyoming and (4) southern Utah. The WA-CB population showed the highest degree of genetic distinctiveness using multiple clustering, ordination, and genetic differentiation analyses. Our results highlight the long-term isolation of the WA-CB population as well as historical isolation of other peripheral populations. We identified signatures of putatively adaptive loci among populations, but no significant gene ontology associated with local adaptation. Our results provide SNP loci for monitoring demography and the consequences of genetic rescue efforts in the admixed WA-CB population.