Programs that manage threatened species in captivity are carefully designed to minimise genetic diversity loss, inbreeding and adaptation to captivity in order to maximise evolutionary potential. But, changes in productivity over generations in captivity can threaten the ability of captive breeding programs to reach their genetic targets and impair the potential of reintroduced captive animals to contribute to wild populations. These long-term changes have not yet been investigated in a zoo species. Marsupials are characterised by short generation times, putting them at particular risk of adaptation to captivity over short time periods. We tested for changes over time in captivity by analysing pedigree data from a nine-year Tasmanian devil insurance population studbook, including 338 animals across 17 breeding sites, and examined seven genetic, biological and management factors affecting reproductive success. We observed a substantial decline in reproductive success with increasing generations in captivity: captive-born females were less likely to produce a litter than wild-born females and when they did, they also produced fewer joeys. Reproductive success also declined as dam age at first breeding increased. The latter result implies a conflict with recommended conservation genetic strategy that aims to limit opportunity for selection and minimise adaptation to captivity by delaying reproduction. We suggest possible reasons for changes in productivity in relation to pedigree-based strategies for the management of captive populations. Our results have broad practical applications for the genetic management of threatened species worldwide; ongoing work will investigate the underlying molecular basis for these observations.