Phylogenetic relationships amongst the robust capuchin monkeys (genus Sapajus) are poorly understood. Morphology-based taxonomies have recognized anywhere from one to twelve different species. The current IUCN (2017) classification lists eight robust capuchins: S. xanthosternos, S. nigritus, S. robustus, S. flavius, S. libidinosus, S. cay, S. apella and S. macrocephalus. Here, we assembled the first phylogenomic data set for Sapajus using ultra-conserved elements (UCEs) to reconstruct a capuchin phylogeny. All phylogenomic analyses strongly supported a deep divergence of Sapajus and Cebus clades within the capuchin monkeys, and provided support for Sapajus nigritus, S. robustus and S. xanthosternos as distinct species. However, the UCE phylogeny lumped the putative species S. cay, S. libidinosus, S. apella, S. macrocephalus, and S. flavius together as a single widespread lineage. A SNP phylogeny constructed from the UCE data was better resolved and recovered S. flavius and S. libidinosus as sister species; however, S. apella, S. macrocephalus, and S. cay individuals were recovered in two geographic clades, from northeastern and southwestern Amazon, rather than clustering by currently defined morphospecies. STRUCTURE analysis of population clustering revealed widespread admixture among Sapajus populations within the Amazon and even into the Cerrado and Atlantic Forest. Difficulty in assigning species by morphology may be a result of widespread population admixture facilitated through frequent movement across major rivers and even ecosystems by robust capuchin monkeys.