Understanding the genetic diversity and evolutionary history of plant pathogens is crucial for effective disease management strategies. Sunflower downy mildew, caused by the oomycete Plasmopara halstedii , is a worldwide threat to the sunflower oil crop. We aimed to explain through phylogenomic studies how downy mildew resistance breakdown occurred recurrently in the last decades in France, leading to new virulence profiles. We assembled high-quality genomes of three founder pathotypes of Pl. halstedii . Performing comparative genomic analyses, population genetics, and phylogenomic analyses, we studied the genomic structure among the 16 reference French pathotypes of Pl. halstedii . We revealed a conserved genomic organisation among pathotypes and a strong synteny with other Peronosporales species. The history of Pl. halstedii invasion in France over the last 60 years was documented by identifying founder strains and their admixture patterns. The emergence of pathotypes with broader virulence spectra and therefore capable of overcoming host resistance was associated with genomic reshuffling. We highlighted genomic mosaicism in admixed pathotypes and identified regions associated with the breakdown of host resistance genes harbouring putative effector genes. Our findings provide insights into evolutionary mechanisms underlying plant pathogen host adaptation, which has implications for a sustainable deployment of multiple resistance genes.