Recent evidence demonstrates genomic and morphological continuity in the Arctic ancestral lineage of dogs. Here, we use the Siberian Husky to investigate the genomic legacy of the northeast Eurasian Arctic lineage and model the deep population history using genome-wide single nucleotide polymorphisms. Utilizing ancient dog-calibrated molecular clocks, we found that at least two distinct lineages of Arctic dogs existed in ancient Eurasia at the end of the Pleistocene. This pushes back the origin of sled dogs in the northeast Siberian Arctic with humans likely intentionally selecting dogs to perform different functions and keeping breeding populations that overlap in time and space relatively reproductively isolated. In modern Siberian Huskies, we found significant population structure based on how they are used by humans, recent European breed introgression in about half of the dogs that participate in races, moderate levels of inbreeding, and fewer potentially harmful variants in populations under strong selection for form and function (show, sled show, and racing populations of Siberian Huskies). As the struggle to preserve unique evolutionary lineages while maintaining genetic health intensifies across pedigreed dogs, understanding the genomic history to guide policies and best practices for breed management is crucial to sustain these ancient lineages and their unique evolutionary identity.