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Summary: West and South Asian populations profoundly influenced Eurasian genetic and cultural diversity. We investigate the genetic history of the Y chromosome haplogroup L1-M22, which, while prevalent in these regions, lacks in-depth study. Robust Bayesian analyses of 165 high-coverage Y chromosomes favor a West Asian origin for L1-M22 ∼20.6 thousand years ago (kya). Moreover, this haplogroup parallels the genome-wide genetic ancestry of hunter-gatherers from the Iranian Plateau and the Caucasus. We characterized two L1-M22 harboring population groups during the Early Holocene. One expanded with the West Asian Neolithic transition. The other moved to South Asia ∼8-6 kya but showed no expansion. This group likely participated in the spread of Dravidian languages. These South Asian L1-M22 lineages expanded ∼4-3 kya, coinciding with the Steppe ancestry introduction. Our findings advance the current understanding of Eurasian historical dynamics, emphasizing L1-M22’s West Asian origin, associated population movements, and possible linguistic impacts.