Abstract Background and Aims Acrocomia is a Neotropical palm genus that recently gained attention for its potential as a multipurpose crop. Among its species, A. aculeata and A. totai stand out for their potential in sustainable biofuel production and ecosystem restoration. Despite their relevance, the genomic structure and domestication history of these species remain poorly understood. This study aims to characterize the genetic structure and diversity of A. aculeata and A. totai across their natural distribution, to understand the biogeographical processes behind their differentiation, and to investigate the domestication history of A. aculeata through a genetic, ecological, archaeobotanical and ethnographic lens. Methods We used double-digest genotyping-by-sequencing to analyse 85 individuals of A. aculeata and 11 of A. totai from nine countries. Genomic structure was assessed using sparse non-negative matrix factorization, discriminant analysis of principal components and neighbour-joining methods. For A. aculeata, we performed ecological niche modelling during the Pliocene and genome scans to identify outlier single nucleotide polymorphisms (SNPs) within the major genetic groups. These results were integrated with archaeobotanical and ethnographic data to contextualize domestication patterns. Key Results We identified nine highly structured genetic clusters with low gene flow, confirming two major gene pools: Central and South America, shaped by Pleistocene–Holocene biogeographical dynamics. Using SNPs under selection, we found three regional clusters in A. aculeata: Central America, Amazonia and southeastern Brazil. Functional annotation revealed lineage-specific genes linked to agronomic traits: disease resistance, dwarfism and fruit development in Central America, and lipid metabolism and transcriptional regulation in South America, which may be related to independent domestication pathways over the past 13 000 years. Conclusions Our findings offer new insights into the evolutionary and biocultural history of Acrocomia, supporting the existence of distinct evolutionary trajectories. These results highlight the species’ potential for sustainable development and emphasize the need for just strategies that include traditional communities in contemporary production systems.