Infectious diseases are unlikely to be the ultimate driver of wildlife extinction due to disease fade-out as a host population declines. One exception is where falling population immunity, as a consequence of fading pathogen endemicity, exposes a threatened species to spillover infection from reservoirs of pathogens in more abundant hosts. Increased vulnerability to stochastic extinction associated with disease might thus be enhanced as an endangered population dwindles. Conservation efforts for the orange-bellied parrot (Neophema chrysogaster), one of the world’s most critically endangered bird species, have been hampered by beak and feather disease virus (BFDV) spillover infection. To understand the vulnerability of orange-bellied parrots to potential reservoirs of infection we analysed BFDV from captive and wild orange-bellied parrot flocks and other wild parrot species in Australia. By identifying genetic stratification of BFDV in reservoir hosts we characterized three separate recent incursions of BFDV into orange-bellied parrots from other wild parrots, which highlight the susceptibility of critically endangered species to multiple threats of pathogen re-emergence. Importantly, this study highlights how loss of endemic circulating BFDV in orange-bellied parrots precipitated repeated spillover into an immunologically naïve population, causing significant disease. The conservation of threatened species must recognise the repercussions of endemic pathogen loss often associated with declining or small population size and there is a need to proactively manage the impoverishment of the microbiome and risk of pathogen spillover into these species.