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Recent molecular studies have clarified the overarching taxonomy of capuchin monkeys, but intraspecific genetic diversity remains unexplored for most capuchin species. One example is Sapajus nigritus, the southernmost capuchin monkey, found in Brazil and Argentina; its phenotypic diversity has been recognized as two geographic subspecies, but the intraspecific genetic structure of this taxon is poorly known. Here, we sampled across most of this species' geographic distribution, producing a newly sequenced data set for genetic analyses that included 78 individuals from 14 populations. We investigated the intraspecific diversity, genetic structure, and evolutionary history using three mitochondrial markers. Our results indicated that S. nigritus populations exhibited high levels of genetic structure. We found strong support for two monophyletic clades within this species with a deep phylogenetic split, and clear separation from other related taxa. Vicariance events seem to have played a prevalent role in shaping S. nigritus genetic differentiation. The Paraíba do Sul River may have driven the deep divergence between southern and northern clades, whereas the Tietê River may have had a weaker, more recent effect on the divergence of populations within the southern clade. Research Highlights: Using mitochondrial markers we found support for two major clades within Sapajus nigritus; the Paraíba do Sul River probably acted as a barrier to drive this deep phylogenetic split, estimated to have occurred at 1.56 MaWe recovered the southern S. nigritus clade as sister to a clade of other Sapajus species (S. cay, apella, macrocephalus, robustus, flavius) rather than northern S. nigritus, emphasizing southern and northern clades as distinct phylogenetic unitsS. nigritus D‐loop analysis showed high pairwise populational genetic differentiation and geographic structure; this D‐loop database can now be used for to help identify the geographical origin of illegally traded animals [ABSTRACT FROM AUTHOR]