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As the first domestic species, dogs likely dispersed with different cultural groups during the Late Pleistocene and Holocene. To test this hypothesis, we analyzed 73 ancient dog genomes, including 17 newly sequenced individuals sampled from East Asia to the West Eurasian Steppe spanning nearly 10,000 years. Our results indicate correlations between the ancestry of dogs and specific ancient human populations from eastern Europe to Eastern Siberia, including Ancient Paleo-Siberians, Eastern hunter-gatherers, East Asians, and Steppe pastoralists. We also identify multiple shifts in the ancestry of dogs that coincide with specific dispersals of hunter-gatherers, farmers, and pastoralists. Combined, our results reveal the long-term and integral role that dogs played in a multitude of human societies.