Abstract Uakari monkeys (genus Cacajao ) are endemic to the Amazon rainforest. These have been divided into two main groups: bald and black, mainly based on phenotypic and ecological differences, for which eight taxonomic species have been described. We present 48 geo-localized high coverage whole genomes from uakaris in wild populations across their habitat range. The resolution in terms of sequencing depth provided by this dataset has allowed us to closely explore the structure and evolutionary past of these populations inhabiting the highly dynamic and diverse Amazon rainforest, unavailable until now. Also, we have refined previous phylogenetic estimates by presenting the first whole genome phylogenies available for Cacajao, which were built based on 1Mb and 250kb windows respectively. In this context, bald and black uakaris showed differing genetic diversity ranges, group-specific non-synonymous variation enriched for pathogen-related pathways, and strong population structure, both among and within species. Despite the latter, connectivity was common inside each group whilst strongly shaped by allopatric barriers. Strikingly, even though their habitat ranges partially overlap, no migration was detected between these two groups. Lastly, demographic inference was performed employing a maximum likelihood approach, with which we i) obtained overall higher effective population size estimates for bald extant and ancestral populations than black in agreement with genetic diversity patterns, and ii) found the evolutionary divergence times in the genus were as old as one million years, depicting a quite recent evolutionary history. With this work we increased the representation of wild non-human primates in genomic studies, particularly that of platyrrhine lineages such as Cacajao .