Understanding how pathogens emerge is essential to bring disease-causing agents under durable human control. Here, we used cross-pathogenicity tests to investigate the changes in life-history traits of the fungal pathogen Venturia inaequalis associated with host-tracking during the domestication of apple and subsequent host-range expansion on the wild European crabapple (Malus sylvestris). Pathogenicity of 40 isolates collected in wild and domesticated ecosystems was assessed on the domesticated apple, its Central Asian main progenitor (M. sieversii) and M. sylvestris. Isolates from wild habitats in the centre of origin of the crop were not pathogenic on the domesticated apple and less aggressive than other isolates on their host of origin. Isolates from the agro-ecosystem in Central Asia infected a higher proportion of plants with higher aggressiveness, on both the domesticated host and its progenitor. Isolates from the European crabapple were still able to cause disease on other species but were less aggressive and less frequently virulent on these hosts than their endemic populations. Our results suggest that the domestication of apple was associated with the acquisition of virulence in the pathogen following host-tracking. The spread of the disease in the agro-ecosystem would also have been accompanied by an increase in overall pathogenicity.