The origin and early dispersal of speakers of Transeurasian languages, i.e., Japanese, Korean, Tungusic, Mongolic and Turkic, is among the most disputed issues of Eurasian population history. A key problem is the relationship between linguistic dispersals, agricultural expansions and population movements. Here we address this question through ‘triangulating’ genetics, archaeology and linguistics in a unified perspective. We report new, wide-ranging datasets from these disciplines, including the most comprehensive Transeurasian agropastoral and basic vocabulary presented to date, an archaeological database of 255 Neolithic and Bronze Age sites from Northeast Asia, and the first collection of ancient genomes from Korea, the Ryukyu islands and early cereal farmers in Japan, complementing previously published genomes from East Asia. Challenging the traditional ‘Pastoralist Hypothesis’, we show that the common ancestry and primary dispersals of Transeurasian languages can be traced back to the first farmers moving across Northeast Asia from the Early Neolithic onwards, but that this shared heritage has been masked by extensive cultural interaction since the Bronze Age. As well as marking significant progress in the three individual disciplines, by combining their converging evidence, we show that the early spread of Transeurasian speakers was driven by agriculture.