The evolutionarily persistent and widespread use of carotenoid pigments in animal coloration contrasts with their biochemical instability. Consequently, evolution of carotenoid-based displays should include mechanisms to accommodate or limit pigment degradation. In birds, this could involve two strategies: (i) evolution of a moult immediately prior to the mating season, enabling the use of particularly fast-degrading carotenoids and (ii) evolution of the ability to stabilize dietary carotenoids through metabolic modification or association with feather keratins. Here, we examine evolutionary lability and transitions between the two strategies across 126 species of birds. We report that species that express mostly unmodified, fast-degrading, carotenoids have pre-breeding moults, and a particularly short time between carotenoid deposition and the subsequent breeding season. Species that expressed mostly slow-degrading carotenoids in their plumage accomplished this through increased metabolic modification of dietary carotenoids, and the selective expression of these slow-degrading compounds. In these species, the timing of moult was not associated with carotenoid composition of plumage displays. Using repeated samples from individuals of one species, we found that metabolic modification of dietary carotenoids significantly slowed their degradation between moult and breeding season. Thus, the most complex and colourful ornamentation is likely the most biochemically stable in birds, and depends less on ecological factors, such as moult timing and migration tendency. We suggest that coevolution of metabolic modification, selective expression and biochemical stability of plumage carotenoids enables the use of unstable pigments in long-term evolutionary trends in plumage coloration.