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The resolution of conservation genetic analyses has been limited until recently due to technological and computational challenges associated with genotyping multiple loci at once. In this review, we focus on how the development of high-throughput genotyping methods have enabled conservation genomics studies of wolves in North America. The gray wolf (Canis lupus) historically had a Holarctic distribution across widely varying environments, yet during the early twentieth century many populations declined due to direct persecution and other anthropogenic disturbances. First, we discuss genetic substructure and adaptive uniqueness among genetically and environmentally defined wolf ecotypes. Second, we focus on the new conservation implications revealed by studies having increased genomic resolution of the dynamics of reintroduced and re-established wolves, specifically Mexican and Pacific Northwest wolves. Mexican wolves, a distinct subspecies of North American wolf that inhabit a small area within the southwestern U.S. and Mexico, remain endangered despite decades since a reintroduction program began. How biologists and management agencies use scientific data to define the historical range of Mexican wolves will be critical to future reintroduction efforts. In the Pacific Northwest, admixture occurs between the distinct and declining coastal wolf ecotype and the more abundant reintroduced interior wolves. If coastal wolves obtain protection, then the Pacific Northwest wolves may also warrant protection. Therefore, more precise policies are needed for the management of admixed populations when one source is protected. We recommend that future conservation efforts should provide full protection for distinct ecotypes, support scientifically rigorous definitions of historical range to inform restoration, and enhance the legal status of admixed populations.