Cultures in humans and other species are maintained through interactions among conspecifics. Declines in population density could be exacerbated by culture loss, thereby linking culture to conservation. We combined historical recordings, citizen science and breeding data to assess the impact of severe population decline on song culture, song complexity and individual fitness in critically endangered regent honeyeaters (Anthochaera phrygia). Song production in remaining wild males varied dramatically, with 27 % singing songs that differed from the regional cultural norm. 12% of males, occurring in areas of particularly low population density, completely failed to sing any species-specific songs and instead sang other species’ songs. Atypical song production was associated with reduced individual fitness, as males singing atypical songs were less likely to pair or nest than males that sang the regional cultural norm. Songs of captive-bred birds differed from those of all wild birds. The complexity of regent honeyeater songs has also declined over recent decades. We therefore provide rare evidence that a severe decline in population density is associated with loss of vocal culture in a wild animal, with concomitant fitness costs for remaining individuals. Loss of culture may be a precursor to extinction in declining populations that learn selected behaviours from conspecifics, and therefore provides a useful conservation indicator.