Biotrophic fungal pathogens are expected to have adapted to their host plants for phenological synchrony, to optimize the possibility of contacts leading to infections. We investigated the patterns and causes of variation in phenological synchrony in the oak-powdery mildew pathosystem, a major disease in natural ecosystems. The study was carried out along an altitudinal gradient, representing a wide temperature range, in mature oak stands. Both sporulation (pathogen infective stage) and oak flushing (host susceptible stage) were delayed with increasing elevation, but with a significantly different sensitivity for the two species. This resulted in a variable host–pathogen synchrony along the gradient. A common garden experiment did not give evidence of among-population genetic differentiation (past adaptation) for fungal phenology. This could be explained by the high phenotypic variation in phenology within host populations, precluding selection on fungal phenology at the population scale, but possibly favouring adaptation at the within-population scale. Phenotypic plasticity was the major cause of the observed variation in the phenology of the fungal populations.