The ecological conditions experienced by wildlife reservoir hosts affect the amount of pathogen they excrete into the environment. This then shapes pathogen pressure, the amount of pathogen available to recipient hosts over space and time, which affects spillover risk. Few systems have data on both long-term ecological conditions and pathogen pressure, yet such data are critical for advancing our mechanistic understanding of ecological drivers of spillover risk. To identify these ecological drivers, we here reanalyze shedding data from a spatially replicated, multi-year study of Hendra virus excretion from Australian flying foxes in light of 25 years of long-term data on changing ecology of the bat reservoir hosts. Using generalized additive mixed models, we show that winter virus shedding pulses, previously considered idiosyncratic, are most pronounced after recent food shortages and in bat populations that have been displaced to novel habitats. We next derive the area under each annual shedding curve (representing cumulative virus excretion) and show that pathogen pressure is also affected by the ecological conditions experienced by bat populations. Finally, we illustrate that pathogen pressure positively predicts observed spillover frequency. Our study suggests that recent ecological conditions of flying fox hosts are shifting the timing, magnitude, and cumulative intensity of Hendra virus shedding in ways that shape the landscape of spillover risk. This work provides a mechanistic approach to understanding and estimating risk of spillover from reservoir hosts in complex ecological systems and emphasizes the importance of host ecological context in identifying the determinants of pathogen shedding.