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Manipur is one of the North-Eastern states of India and it lies on the ancient silk route and serves as a meeting point between the Southeast Asia and South Asia. The origin and migration histories of Naga and Kuki tribal populations have not been clearly understood. Moreover, Kukis have been traced to two different ancestries, which have created confusion among the people. The present study examined genomic affinities and differentiation of the Naga and Kuki tribal populations of Manipur, Northeast India. Twenty autosomal markers (Eight Alu InDels, and twelve Restriction Fragment Length Polymorphisms) were analysed. Findings showed genetic differences between Naga and Kuki tribal populations with respect to the allele distribution pattern which was substantiated by genetic differentiation (GST 5.2%) and molecular variance (AMOVA) where the highest percentage of among group variances was observed between Naga and Kuki tribal groups (7.09%). However, genetic similarity with respect to allele distribution pattern in most of the loci were seen among their respective groups (Rongmei and Inpui; Thadou and Vaiphei). Rongmei and Inpui tribal populations (Naga group) belong to Naga-Bodo linguistic group and Thadou and Vaipei (Kuki group) belong to Northern Kuki-Chin linguistic group suggesting that genetic similarities may not be independent of linguistic affinities. Despite differential genetic affinities, both Naga and Kuki tribal populations in Manipur show proximity with Southeast Asian populations and Northeast Indian populations than with other Indian populations and global populations taken for comparison.