As the continent of origin for our species, Africa harbours the highest levels of diversity anywhere on Earth. This trove of diversity provides rich opportunities to discover unknown genomic variation and explore how human populations have moved and interacted on the continent over thousands of years. However, many regions of Africa remain under-sampled. Here we present the first collection of whole genomes from Angola and Mozambique, enabling the construction of a high-quality reference variation catalogue including three million novel SNPs. Leveraging the power and flexibility of whole-genome sequencing data, we model the development and continuity of Bantu-population structure through time, admixture events involving source populations from these regions across sub-Saharan Africa, and the heterogeneous population histories of Western and South-Eastern Bantu-speakers. In contrast to depictions of the Bantu expansion as a single, continuous macro-event, we recover evidence of admixture among distinct Bantu-speaking groups in South-Eastern Africa and bring together concordant patterns from linguistics and archaeology to paint a more complex picture of Iron-Age migrations into the region. Moreover, we generate reference panels that better represents the complete diversity of African populations involved in the Atlantic slave trade, improving imputation accuracy in African Americans and Brazilians over the 1000 Genomes Project panel alone. This study fills important gaps in the current record of global genetic diversity and informs on the most significant demographic events in the recent history of Africa. We anticipate that our collection of genomes will form the foundation for future genomic healthcare initiatives involving under-represented communities in Angola and Mozambique.