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The peopling history of North Asia remains largely unexplored due to the limited number of ancient genomes analyzed from this region. Here, we report genome-wide data of ten individuals dated to as early as 7,500 years before present from three regions in North Asia, namely Altai-Sayan, Russian Far East, and the Kamchatka Peninsula. Our analysis reveals a previously undescribed Middle Holocene Siberian gene pool in Neolithic Altai-Sayan hunter-gatherers as a genetic mixture between paleo-Siberian and ancient North Eurasian (ANE) ancestries. This distinctive gene pool represents an optimal source for the inferred ANE-related population that contributed to Bronze Age groups from North and Inner Asia, such as Lake Baikal hunter-gatherers, Okunevo-associated pastoralists, and possibly Tarim Basin populations. We find the presence of ancient Northeast Asian (ANA) ancestry-initially described in Neolithic groups from the Russian Far East-in another Neolithic Altai-Sayan individual associated with different cultural features, revealing the spread of ANA ancestry ∼1,500 km further to the west than previously observed. In the Russian Far East, we identify 7,000-year-old individuals that carry Jomon-associated ancestry indicating genetic links with hunter-gatherers in the Japanese archipelago. We also report multiple phases of Native American-related gene flow into northeastern Asia over the past 5,000 years, reaching the Kamchatka Peninsula and central Siberia. Our findings highlight largely interconnected population dynamics throughout North Asia from the Early Holocene onward., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2022 Elsevier Inc. All rights reserved.)