Understanding how emerging viruses persist in bat populations is a fundamental step to understand the processes by which viruses are transmitted from reservoir hosts to spillover hosts. Hendra virus, which has caused fatal infections in horses and humans in eastern Australia since 1994, spills over from its natural reservoir hosts, Pteropus bats (colloquially known as flying foxes). It has been suggested that the Hendra virus maintenance mechanism in the bat populations might be implicated with their metapopulation structure. Here, we examine whether a metapopulation consisting of black flying fox (P. alecto) colonies that are smaller than the critical community size can maintain the Hendra virus. By using the Gillespie algorithm, stochastic mathematical models were used to simulate a cycle, in which viral extinction and recolonisation were repeated in a single colony within a metapopulation. Given estimated flying fox immigration rates, the simulation results showed that recolonisation occurred more frequently than extinction, which indicated that infection would not go extinct in the metapopulation. Consequently, this study suggests that a collection of transient epidemics of Hendra virus in numerous colonies of flying foxes in Australia can support the long-term persistence of the virus at the metapopulation level.