Coronaviruses were responsible for the global outbreaks of severe acute respiratory syndrome (SARS) in 2003 and 2004, and Middle East respiratory syndrome (MERS) in 2012. Bats have since been identified as the natural hosts for a number of novel coronaviruses, including the likely ancestors to SARS and MERS coronaviruses. It is essential for Australia’s biosecurity preparedness, and for the broader understanding of this previously unknown group of viruses, that coronaviruses in bats in our region are identified, characterised and their ecology understood. 2,195 bats collected from Australia and neighbouring countries between 1997 and 2009 were tested for evidence of coronavirus infection. The study identified coronaviruses belonging to two genera (Alpha- and Betacoronavirus) in Australian bats, and serological evidence of infection in other bats from East Timor, Indonesia, Malaysia and Papua New Guinea. It also identified the interspecies transmission of a variant of the alphacoronavirus Miniopterus bat coronavirus HKU8 from Miniopterus spp to bats of the genus Rhinolophus, supporting the hypothesis that bats from this genus are more likely to foster host shifts and pose a risk for the emergence of other bat coronaviruses. A two year longitudinal study of Miniopterus spp between 2006 and 2008 was used to collect data and develop a model hypothesis of the infection dynamics of an Alphacoronavirus. The findings suggested that bats have an anamnestic (immunological) memory which limits secondary coronavirus infections with a stronger and more rapid production of antibodies, compared to a primary infection. Finally, a modified mark/recapture study on a maternal population of Myotis macropus identified that individual bats were infected with a novel unclassified putative Alphacoronavirus for up to 11 weeks. The observed pattern of infection supports not only a hypothesis of persistent coronavirus infection in bats, but also suggests that acute infection, and intermittent viral is possible.