Anthropogenic environmental change is often implicated in the emergence of new zoonoses from wildlife;however, there is little mechanistic understanding of these causal links. Here, we examine the trans-mission dynamics of an emerging zoonotic paramyxovirus, Hendra virus (HeV), in its endemic host,AustralianPteropusbats (fruit bats or flying foxes). HeV is a biosecurity level 4 (BSL-4) pathogen,with a high case-fatality rate in humans and horses. With models parametrized from field and laboratorydata, we explore a set of probable contributory mechanisms that explain the spatial and temporal patternof HeV emergence; including urban habituation and decreased migration—two widely observed changesin flying fox ecology that result from anthropogenic transformation of bat habitat in Australia. Urbanhabituation increases the number of flying foxes in contact with human and domestic animal populations,and our models suggest that, in addition, decreased bat migratory behaviour could lead to a decline inpopulation immunity, giving rise to more intense outbreaks after local viral reintroduction. Ten of the14 known HeV outbreaks occurred near urbanized or sedentary flying fox populations, supportingthese predictions. We also demonstrate that by incorporating waning maternal immunity into ourmodels, the peak modelled prevalence coincides with the peak annual spill-over hazard for HeV. Theseresults provide the first detailed mechanistic framework for understanding the sporadic temporal patternof HeV emergence, and of the urban/peri-urban distribution of HeV outbreaks in horses and people.