The ecological and evolutionary dynamics of species are influenced by spatiotemporal variation in population size. Unfortunately, we are usually limited in our ability to investigate the numerical dynamics of natural populations across large spatial scales and over long periods of time. Here we combine mechanistic and statistical approaches to reconstruct continuous-time infection dynamics of an obligate fungal pathogen on the basis of discrete-time occurrence data. The pathogen, Podosphaera plantaginis, infects its host plant, Plantago lanceolata, in a metapopulation setting where the presence of the pathogen has been recorded annually for 6 years in approximately 4,000 host populations across an area of 50 km x 70 km in Finland. The dynamics are driven by strong seasonality, with a high extinction rate during winter and epidemic expansion in summer for local pathogen populations. We are able to identify with our model the regions in the study area where overwintering has been most successful. These overwintering sites represent foci that initiate local epidemics during the growing season. There is striking heterogeneity at the regional scale in both the overwintering success of the pathogen and the encounter intensity between the host and the pathogen. Such heterogeneity has profound implications for the coevolutionary dynamics of the interaction.