The Australian wheat stem rust (Puccinia graminis f. sp. tritici) population was shaped by the introduction of four exotic incursions into the country. It was previously hypothesized that at least two of these (races 326-1,2,3,5,6 and 194-1,2,3,5,6 first detected in 1969) had an African origin and moved across the Indian Ocean to Australia on high-altitude winds. We provide strong supportive evidence for this hypothesis by combining genetic analyses and complex atmospheric dispersion modelling. Genetic analysis of 29 Australian and South African P. graminis f. sp. tritici races using microsatellite markers confirmed the close genetic relationship between the South African and Australian populations, thereby confirming previously described phenotypic similarities. Lagrangian Particle Dispersion Model simulations using finely resolved meteorological data showed that long distance dispersal events between southern Africa and Australia are indeed possible, albeit rare. Simulated urediniospore transmission events were most frequent from central South Africa (viable spore transmission on ~7% of all simulated release days) compared with other potential source regions in southern Africa. The study acts as a warning of possible future P. graminis f. sp. tritici dispersal events from southern Africa to Australia, which could include members of the Ug99 race group, emphasizing the need for continued surveillance on both continents.