Genetic analysis can provide valuable information for conservation programmes by unravelling the demographic trajectory of populations, estimating effective population size or inferring genetic differentiation between populations. Here, we investigated the genetic differentiation within Snowy Owls Bubo scandiacus in North America, a species identified as vulnerable by the IUCN, to (1) quantify connectivity among wintering areas, (2) evaluate current genetic diversity and effective population size, and (3) infer changes in the historical effective population size changes from the last millennia to the recent past. The Snowy Owl, a highly mobile top predator, breeds across the Arctic tundra, a region especially sensitive to current climate change. Using single‐nucleotide polymorphism (SNP)‐based analyses on Snowy Owls sampled across the North American non‐breeding range, we found an absence of genetic differentiation among individuals located up to 4650 km apart. Our results suggest high genetic intermixing and effective dispersal at the continental scale despite documented philopatry to non‐breeding sites in winter. Reconstructing the population demographic indicated that North American Snowy Owls have been steadily declining since the Last Glacial Maximum c. 20 000 years ago, and concurrently with global increases in temperature. Conservation programmes should now consider North American Snowy Owls a single, genetically homogeneous continental‐wide population which is probably sensitive to the long‐term global warming occurring since the Last Glacial Maximum.