The ecological conditions experienced by wildlife reservoirs affect infection dynamics and thus the distribution of pathogen excreted into the environment, which have been hypothesized to shape risks of zoonotic spillover. However, few systems have data on both long-term ecological conditions and pathogen excretion to advance mechanistic understanding and test environmental drivers of spillover risk. We here analyze three years of Hendra virus data from nine Australian flying fox roosts with covariates derived from long-term studies of bat ecology. We show that the magnitude of winter pulses of viral excretion, previously considered idiosyncratic, are most pronounced after recent food shortages and in bat populations displaced to novel habitats. We further show that cumulative pathogen excretion over time is shaped by bat ecology and positively predicts spillover frequency. Our work emphasizes the role of reservoir host ecology in shaping pathogen excretion and provides a new approach to estimate spillover risk.