Erysiphe alphitoides causes oak powdery mildew, an example of disease in a wild perennial plant that has shown dramatic changes over a century in Europe. There are several hypotheses for this: pathogen evolution towards lower virulence, a reciprocal increase in oak population resistance, and environmental factors. We show that understanding the pathosystem requires accounting of both seasonality and the occurrence of a pathogen complex, with several cryptic fungal species differing in their life-history traits. Observational data suggest that severity of annual epidemics is linked to interannual pathogen transmission, including winter survival and the infection success of the primary inoculum in spring. Climate-driven phenological synchrony between host and pathogen in spring appears to be critical. Several cryptic Erysiphe species are associated with the disease and co-occur at multiple spatial scales. A semi-discrete model combining a SIR model in the epidemic phase and a discrete-time model between years, based on a within–between season transmission trade-off, describes seasonality and the coexistence of pathogen species. We discuss model refinement by the introduction of host population age classes and other modelling approaches for the evolution of pathogen virulence and host resistance in a changing environment.