Historic transposon mobilisation waves create distinct pools of adaptive variants in a major crop pathogen

Transposable elements (TEs) shape host-pathogen interactions and contribute to antimicrobial resistance, but how adaptive TEs arise in populations and how historical contingencies affect TE dynamics remains unclear. Fungal crop pathogens provide unique frameworks to address such questions due to spatially explicit sampling and well-characterized niches. We characterise TE evolutionary dynamics in 1953 publicly available genomes across the global distribution range of the major wheat pathogen Zymoseptoria tritici. We characterise genomic diversity, benchmark methods to infer TE insertion polymorphism, and assess TEs as a source of adaptive variation. Across ~3.2 million annotated TE loci, we find substantial variation in TE content within and across populations. TE activity surged during the pathogen’s expansion from the Middle East, with distinct activity profiles in derived populations. TE-mediated adaptation emerged from waves of TE mobilization, with the highest TE activity observed over as little as 25 years. 45 TE loci within 1 kb of 49 host genes show local adaptation signatures, likely related to adaptation to antifungals and the plant host environment. This work highlights the power of vast genomic datasets to unravel intraspecies TE invasion histories and pinpoint factors driving recent adaptation and argues for deep population-level TE surveys to uncover molecular drivers of adaptive evolution.