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The reservoir of Ebola virus (EBOV) has remained a mystery since the first recorded zoonotic epidemic in 1976. While recent outbreaks have revealed much about the epidemiological dynamics that sustain human-to-human transmission, the mechanisms by which the virus persists between epidemics are unknown. Observations of extreme EBOV evolutionary rate heterogeneity in humans suggest latency is an important, yet untested, factor in persistence between epidemics. We here explicitly model latency with a novel phylogenetic approach to characterise the natural history of EBOV and, by extension, its reservoir. We find evidence that EBOV undergoes extended periods (i.e., possibly decades) of quiescence in the reservoir. Accounting for these dynamics significantly changes our understanding of EBOV’s evolutionary past and its geographic spread through Central Africa.