Humans have relied on animal fur for centuries, yet fur farming only began recently during the mid-19th Century. Little is known about this incipient domestication or the genomic processes involved. Domestication may involve founder effects, population bottlenecks and low population size, which, when combined with intense artificial selection, lead to inbreeding, a limited gene pool and reduced fitness. The arctic fox (Vulpes lagopus) has been farmed intensively since the early 1900s and has been artificially selected for economic phenotypes. We investigated the origin of these lineages and the genomic consequences of intensive farming by comparing the genomes of farmed and wild arctic foxes from across their range. Our research indicates recent inbreeding through long Runs of Homozygosity and reduced genomic variation in farmed foxes relative to their respective wild populations. We identified a coastal ecotype origin for all Fennoscandian farmed arctic foxes, aligning them phylogenetically with the wild Icelandic population, a geographically isolated and phenotypically distinct coastal lineage. The depleted genome-wide heterozygosity and increased recent inbreeding in farmed fox lineages is consistent with a heavy consequence of domestication, shedding light on the demographic history and genomic consequences of human manipulation. We highlight the need for increased genomic investigations into fur farm populations to understand the incipient domestication process and uncover the cost of intense farming. The genomic consequences of domestication must be considered in the management of fur farms, with actionable steps needed to prevent descendants of escaped farmed foxes from polluting the gene pool in the wild through introgression.