AbstractHarmonia axyridis is an invasive beetle (Coleoptera: Coccinellidae), native to Asia, that has established on four continents beyond its native range and was first observed in South Africa in 2001. Using microsatellite data and a comprehensive geographic coverage of international (17 locations) and South African (14 locations) beetle samples, we inferred the source of colonists invading South Africa and the beetle’s movement within the country. Genetic structure analyses suggest that this species’ populations in South Africa are derived from admixture between beetles originating from eastern North America (which acted as a bridgehead population) and another population not directly sampled in our study. Genetic admixture prior its invasion into South Africa, along with the possibility of multiple introductions from the bridgehead population, may explain the high genetic diversity estimates for South African H. axyridis (HE = 0.582–0.625) compared to beetles from the native range (HE = 0.440–0.636). Harmonia axyridis appear to be frequently exchanging genetic material across South Africa, with no clear genetic structure between sampled locations. However, evidence of weak isolation-by-distance within South Africa suggests that beetles are dispersing less frequently between locations that are furthest apart. This study supports previous findings on global invasion pathways in this species but provides new insights in the context of the invasion in South Africa. We highlight how mixing of distinct lineages from divergent origins prior to the invasion into South Africa has augmented genetic diversity in the region. The high dispersal rates and large effective population sizes inferred from genetic markers suggest that slowing the spread or reducing population abundances of the species in South Africa will be challenging without an integrated, multi-faceted management approach.