Bats host a high diversity of coronaviruses, including betacoronaviruses that have caused outbreaks and pandemics in humans and other species. Here, we study the spatiotemporal dynamics of co-circulating coronaviruses in Pteropus spp bats (flying foxes) in eastern Australia over a three-year period across five roost sites (n = 2537 fecal samples). In total, we identify six betacoronavirus clades, all within the nobecovirus subgenus. Genome sequencing supports overall clade assignments, however, also demonstrates the important role recombination has played in both the long-term and contemporary evolution of these viruses. Using a statistical framework that integrates individual and population level data, we assess the variability in prevalence of viral clades over space and time. Coronavirus infections and co-infections are highest among juveniles and subadults, particularly around the time of weaning. The overlapping shedding dynamics across multiple clades suggest opportunities for recombination, especially in younger bats. Understanding the ecological and host-viral drivers of these seasonally dynamic infections, co-infections, and recombination events will inform future predictive frameworks for coronavirus emergence in humans and other animals.