The bean beetle Callosobruchus maculatus is a worldwide generalist legume seed pest, present in the tropics and subtropics. Despite its economic importance, little is known about the population structure and migration patterns of this bruchid beetle in its continent of origin, both at local and regional scales. Gaining knowledge in the demographic processes experienced by C. maculatus, in particular in its native area, might give clues to understand evolutionary forces that have driven its expansion in traditional agroecosystems. Here, we analyze the genetic structure of 23 African populations of C. maculatus located in eleven different countries, using nuclear (28S) and mitochondrial (CytB) markers, and further apply phylogenetic and demographic analyses. The 28S sequences showed low genetic variability. In contrast, the analysis of CytB indicated significant genetic differentiation between most populations, suggesting low levels of gene flow, even at a reduced spatial scale. The results obtained from the estimation of various demographic parameters suggest evidence of recent population expansion, in agreement with a scenario of long-distance dispersal through trade of legume seeds for human consumption and population growth related to its pest nature. Overall, our results show that biogeography, isolation processes and human-mediated dispersal events drive the genetic structure of this pest in Africa.