In the last two decades, monkeypox outbreaks in human populations in Africa and North America have reminded us that smallpox is not the only poxvirus with potential to cause harm in human populations. Monkeypox transmission is sustained in animal reservoirs, and animal–human contacts are responsible for sporadic outbreaks in humans. Here, we develop and analyze a deterministic epizootic (animal-based) transmission model capturing disease dynamics in an animal population, disease dynamics in an age-structured human population, and their coupling through animal–human contacts. We develop a single-patch model as well as a two-patch meta-population extension. We derive mathematical expressions for the basic reproduction number, which governs the likelihood of a large outbreak. We also investigate the effectiveness of culling strategies and the impact of changes in the animal–human contact rate. Numerical analysis of the model suggests that, for some parameter values, culling can actually have the counter-productive outcome of increasing monkeypox infection in children, if animal reproduction is a density-dependent process. The likelihood of this happening, as well as the prevalence of monkeypox in humans, depends sensitively on the animal–human contact rate. We also find that ignoring age structure in human populations can lead to overestimating the transmissibility of monkeypox in humans. The effectiveness of monkeypox control strategies such as culling can strongly depend on the details of demography and epidemiology in the animal reservoirs that sustain it. Therefore, to better understand how to prevent and control monkeypox outbreaks in humans, better empirical data from wild animal populations where monkeypox is endemic must be collected, and these data must be incorporated into highly structured theoretical models.