Insects are considered promising candidates for improving agronomic sustainability. Contrary to conventional livestock, however, genetic resources of farmed insects remain poorly characterized. We genotyped almost 3,000 black soldier fly (BSF) specimens from 150 wild and captive populations collected in 57 countries worldwide with newly developed microsatellite markers, providing individual genetic fingerprints throughout. Substantial global population genetic structure was detected by various complementary approaches such as analyses of molecular variance, pairwise population differentiation, isolation by distance, cluster analyses, and coalescence-based modelling, which further revealed complex sub-structuring shaped by naturally derived geographic distribution and human-mediated breed formation. In-depth reconstruction of the evolutionary history of the BSF using our novel highly resolving molecular tool kit infers ancient indigenous range expansions emanating from genetic hotspots within the Americas, and further dynamic demographic trajectories to all other non-native continents in recent history, resulting in pronounced diversification of genetically unique wild lineages via colonization from single-sources or intra specific admixture events. Conversely, globally predominant captive populations show reduced genetic diversity and, despite featuring distinct breeding-mediated footprints, trace back to a single origin that exhibits marked signatures of domestication. Fuelled by common mass-rearing operations, presently ongoing introgression between commercialized domesticated strains and wild populations was found to threaten the genetic integrity of local populations in some regions. Our comprehensive worldwide population genetic inventory of the BSF provides a benchmark for necessary investigation of this fly’s evolutionary ecology, and particularly allows fast and reliable genetic characterization in applied BSF research, with implications on harnessing the potential of this insect for solving urgent socio-economic challenges