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Objective: To describe the population structure of the 48‐bp variable number of tandem repeats (VNTR), located in exon 3 of the dopamine receptor D4 gene (DRD4), in 41 Tarahumara from northern Mexico, 20 Mixe from southern Mexico, and 169 people from Mexico City. Methods: Genotypes for the DRD4‐VNTR were determined, from which 15 Tarahumara, eight Mixe, and 37 urban homozygous individuals were sequenced. Repeat‐allele frequencies were compared with other world populations. Results: The DRD4‐VNTR variation in Mexico City appeared similar to the world mean. For the Mixe and Maya, DRD4‐VNTR diversity appeared closer to South American groups whereas the Tarahumara were similar to North American groups. People from Mexico City and the Mixe exhibited attributes of a large and admixed population and an isolated population, respectively. The Tarahumara showed endogamy associated with a substructure as suggested by a preliminary regional differentiation. For the DRD4‐VNTR and/or the adjacent 5′‐173 bp sequence, the three populations exhibited negative Tajima's D. Two new VNTR haplotypes were discovered: one in Mexico City and another among the Tarahumara. Conclusions: A differentiation in the DRD4‐VNTR of global relevance occurs between northern and southern populations of Mexico suggesting that the Mexican Trans‐volcanic Belt has been a major frontier for human dispersion in the Americas. Ancient trespass of this barrier appears thus related to a major change in the population structure of the DRD4‐VNTR. Distinctive and independent patterns of DRD4‐VNTR diversity occur among the two Mexican indigenous populations by a still undefined combination of drift and selection. Am. J. Hum. Biol. 26:682–689, 2014. © 2014 Wiley Periodicals, Inc. [ABSTRACT FROM AUTHOR]