Host-pathogen interactions play an important role in shaping ecosystems with many fundamental and applied implications. However, many aspects of the processes, consequences and mechanisms of these antagonistic interactions are still unknown. Evolutionary theory hypothesizes that quantitative plant resistance (QPR) enhances pathogen pathogenicity, therefore, threatening ecological function and sustainability but this hypothesis has rarely been tested empirically. Here, we present results from an eco-evolutionary study of a quantitative plant-pathogen interaction using 16 potato varieties and >2000 Phytophthora infestans strains. Twelve functional traits in a subset (>300 strains) of the P. infestans populations derived from these varieties were compared. Our results indicate that QPR enhances pathogen pathogenicity and facilitates pathogen adaptation to other disease management attempts including the deployment of qualitative plant resistance and the application of fungicides, and to environmental and chemical stresses including salinity, UV radiation, H₂O₂, heat and cold. QPR also increases pathogen spore production and potential of sexual recombination thereby enhancing the generation of new variation for adaptation. Genome-wide analyses indicate that the observed patterns of functional variation result from increased selection from potato varieties with higher QPR and that a substantial portion of genome are involved in the adaptation genetically and epigenetically. Our results highlight a potential risk to ecological function and resilience associated with continuing deployment of QPR, particularly under future climate conditions and are expected to stimulate further investigation into this important phenomenon with many host-pathogen systems.