The characterization of the structure of southern Africa populations has been the subject of numerous genetic, medical, linguistic, archaeological and anthropological investigations. Current diversity in the subcontinent is the result of complex episodes of genetic admixture and cultural contact between the early inhabitants and the migrants that have arrived in the region over the last 2,000 years, with some of the variation present in the past being now lost as the result of cultural and demographic assimilation by surrounding populations. Here we analyze 1,856 individuals from 91 populations, comprising novel and available genotype data to characterize the genetic ancestry profiles of southern African populations. Combining local ancestry and allele frequency analyses we identify a tripartite, ancient, Khoesan-related genetic structure, which correlates with geography, but not with linguistic affiliation or subsistence strategy. The fine mapping of these components in southern African populations reveals admixture dynamics and episodes of cultural reversion involving several Khoesan groups and highlights different mixtures of ancestral components in Bantu speakers and Coloured individuals.