Bats and birds live substantially longer on average than non-flying mammals of similar body size. The combination of small body size, high metabolic rates, and long lifespan in bats and birds would not seem to support oxidative theories of ageing that view senescence as the gradual accumulation of damage from metabolic byproducts. However, large-scale comparative analyses and laboratory studies on a few emerging model species have identified multiple mechanisms for resisting oxidative damage to mitochondrial DNA and cellular structures in both bats and birds. Here we review these recent findings, and suggest areas in which additional progress on ageing mechanisms can be made using bats and birds as novel systems. New techniques for determining the age of free-living, wild individuals, and robustly supported molecular phylogenies, are under development and will improve the efforts of comparative biologists to identify ecological and evolutionary factors promoting long lifespan. In the laboratory, greater development of emerging laboratory models and comparative functional genomic approaches will be needed to identify the molecular pathways of longevity extension in birds and bats.