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Secondary contact between crops and their wild relatives poses a threat to wild species, not only through gene flow between plants, but also through the dispersal of crop pathogens and genetic exchanges involving these pathogens, particularly those that have become more virulent by indirect selection on resistant crops, a phenomenon known as "pestification." Joint analyses of wild and domesticated hosts and their pathogens are essential to address this issue, but such analyses remain rare. We used population genetics approaches, demographic inference and pathogenicity tests on host–pathogen pairs of wild or domesticated apple trees from Central Asia and their main fungal pathogen, Venturia inaequalis, which itself has differentiated agricultural and wild‐type populations. We confirmed the occurrence of gene flow from cultivated (Malus domestica) to wild (Malus sieversii) apple trees in Asian forests, potentially threatening the persistence of Asian wild apple trees. Pathogenicity tests demonstrated the pestification of V. inaequalis, the agricultural‐type population being more virulent on both wild and domesticated trees. Single nucleotide polymorphism (SNP) markers and the demographic modelling of pathogen populations revealed hybridization following secondary contact between agricultural and wild‐type fungal populations, and dispersal of the agricultural‐type pathogen population in wild forests, increasing the threat of disease in the wild apple species. We detected an SNP potentially involved in pathogen pestification, generating an early stop codon in a gene encoding a small secreted protein in the agricultural‐type fungal population. Our findings, based on joint analyses of paired host and pathogen data sets, highlight the threat posed by cultivating a crop near its centre of origin, in terms of pestified pathogen invasions in wild plant populations and introgression in the wild‐type pathogen population. [ABSTRACT FROM AUTHOR]