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Multinational epidemics of emerging infectious diseases are increasingly common, due to anthropogenic pressure on ecosystems and the growing connectivity of human populations. Early and efficient vaccination can contain outbreaks and prevent mass mortality, but optimal vaccine stockpiling strategies are dependent on pathogen characteristics, reservoir ecology, and epidemic dynamics. Here, we model major regional outbreaks of Nipah virus and Middle East respiratory syndrome, and use these to develop a generalized framework for estimating vaccine stockpile needs based on spillover geography, spatially-heterogeneous healthcare capacity and spatially-distributed human mobility networks. Because outbreak sizes were highly skewed, we found that most outbreaks were readily contained (median stockpile estimate for MERS-CoV: 2,089 doses; Nipah: 1,882 doses), but the maximum estimated stockpile need in a highly unlikely large outbreak scenario was 2–3 orders of magnitude higher (MERS-CoV: ~87,000 doses; Nipah ~ 1.1 million doses). Sensitivity analysis revealed that stockpile needs were more dependent on basic epidemiological parameters (i.e., death and recovery rate) and healthcare availability than any uncertainty related to vaccine efficacy or deployment strategy. Our results highlight the value of descriptive epidemiology for real-world modeling applications, and suggest that stockpile allocation should consider ecological, epidemiological, and social dimensions of risk.