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Abstract Fusarium head blight (FHB) is one of the most destructive wheat diseases worldwide. To understand the impact of human migration and changes in agricultural practices on crop pathogens, here population genomic analysis with 245 representative strains from a collection of 4,427 field isolates of Fusarium asiaticum, the causal agent of FHB in Southern China is conducted. Three populations with distinct evolution trajectories are identifies over the last 10,000 years that can be correlated with historically documented changes in agricultural practices due to human migration caused by the Southern Expeditions during the Jin Dynasty. The gradual decrease of 3ADON‐producing isolates from north to south along with the population structure and spore dispersal patterns shows the long‐distance (>250 km) dispersal of F. asiaticum. These insights into population dynamics and evolutionary history of FHB pathogens are corroborated by a genome‐wide analysis with strains originating from Japan, South America, and the USA, confirming the adaptation of FHB pathogens to cropping systems and human migration.