The current COVID-19 pandemic emphasises the dramatic consequences of emerging zoonotic pathogens and stimulates the need for an assessment of the evolution and natural cycle of such microbes in a “One Health” framework. A number of recent studies have revealed an astonishing diversity of bat-borne coronaviruses, including in insular environments, which can be considered as simplified biological systems suited for the exploration of the transmission cycles of these viruses in nature. In this work, we present two new lineages of Alphacoronaviruses detected by screening the only two extant New Zealand bat species: the lesser short-tailed bat (Mystacina tuberculata) and the long-tailed bat (Chalinolobus tuberculatus). Infection prevalence reaching 60% in long-tailed bats makes this host-pathogen model relevant for the investigation of maintenance mechanisms in a bat reservoir with peculiar physiological adaptations to temperate climates. A phylogenetic analysis shows that these viral lineages do cluster with coronaviruses hosted by bat sister species from Australia, supporting co-diversification processes. These patterns provide an interesting framework for further research aiming at elucidating the natural history and biological cycles of bat-borne coronaviruses.