Fungal pathogens cause devastating disease in crops. Understanding the evolutionary origin of pathogens is essential to the prediction of future disease emergence and the potential of pathogens to disperse. The fungus Pyrenophora teres f. teres causes net form net blotch (NFNB), an economically significant disease of barley. In this study, we have used 104 P. teres f. teres genomes from four continents to explore the population structure and demographic history of the fungal pathogen. We showed that P. teres f. teres is structured into populations that tend to be geographically restricted to different regions. Using Multiple Sequentially Markovian Coalescent and machine learning approaches we demonstrated that the demographic history of the pathogen correlates with the history of barley, highlighting the importance of human migration and trade in spreading the pathogen. Exploring signatures of natural selection, we identified several population-specific selective sweeps that colocalized with genomic regions enriched in putative virulence genes, and loci previously identified as determinants of virulence specificities by quantitative trait locus analyses. This reflects rapid adaptation to local hosts and environmental conditions of P. teres f. teres as it spread with barley. Our research highlights how human activities can contribute to the spread of pathogens that significantly impact the productivity of field crops.