Massive gene flow between crops and their wild relatives may threaten the genetic integrity of wild species. Such threats are now well documented, but little is known about indirect consequences involving the spillover of crop pathogens to wild plants or introgression between crop and wild pathogens. To address these questions, we used population genetics approaches, demographic inference and pathogenicity tests on host-pathogen pairs composed of wild or domesticated apple trees of Central Asia and their fungal pathogen, Venturia inaequalis , itself showing differentiated agricultural-type and wild-type populations. We confirmed the occurrence of gene flow from cultivated to wild apple trees in Asian forests, threatening the Asian wild apple genetic integrity. SNP markers and demographic modeling revealed the occurrence of a secondary contact followed by hybridization between agricultural-type and wild-type fungal pathogen populations, and the dispersal of the agricultural-type pathogen in wild forests. We detected a SNP predicting the ability of the fungus to parasitize the different host populations, which induced an early stop codon in a gene coding for a small secreted protein in the agricultural-type fungal population, thus representing a putative avirulence gene which function loss would enable to parasitize cultivated apples. Pathogenicity tests in fact revealed the pestification of V. inaequalis , with higher virulence of the agricultural-type population on both wild and domesticated trees. Our findings highlight the threat posed by cultivating a crop near its center of origin, with the invasion of a pestified pathogen on wild plants and introgression in the wild-type pathogen.