Understanding patterns of genetic diversity is a crucial component of medical research in Africa. Here we use haplotype-based population genetics inference to describe gene-flow and admixture in a collection of 48 African groups with a focus on the major populations of the sub-Sahara. Our analysis presents a framework for interpreting haplotype diversity within and between population groups and provides a demographic foundation for genetic epidemiology in Africa. We show that coastal African populations have experienced an influx of Eurasian haplotypes as a series of admixture events over the last 7,000 years, and that Niger-Congo speaking groups from East and Southern Africa share ancestry with Central West Africans as a result of recent population expansions associated with the adoption of new agricultural technologies. We demonstrate that most sub-Saharan populations share ancestry with groups from outside of their current geographic region as a result of large-scale population movements over the last 4,000 years. Our in-depth analysis of admixture provides an insight into haplotype sharing across different geographic groups and the recent movement of alleles into new climatic and pathogenic environments, both of which will aid the interpretation of genetic studies of disease in sub-Saharan Africa.