The broad palette of feather colours displayed by birds serves diverse biological functions, including communication and camouflage. Fossil feathers provide evidence that some avian colours, like black and brown melanins, have existed for at least 160 million years (Myr), but no traces of bright carotenoid pigments in ancient feathers have been reported. Insight into the evolutionary history of plumage carotenoids may instead be gained from living species. We visually surveyed modern birds for carotenoid-consistent plumage colours (present in 2956 of 9993 species). We then used high-performance liquid chromatography and Raman spectroscopy to chemically assess the family-level distribution of plumage carotenoids, confirming their presence in 95 of 236 extant bird families (only 36 family-level occurrences had been confirmed previously). Using our data for all modern birds, we modelled the evolutionary history of carotenoid-consistent plumage colours on recent supertrees. Results support multiple independent origins of carotenoid plumage pigmentation in 13 orders, including six orders without previous reports of plumage carotenoids. Based on time calibrations from the supertree, the number of avian families displaying plumage carotenoids increased throughout the Cenozoic, and most plumage carotenoid originations occurred after the Miocene Epoch (23 Myr). The earliest origination of plumage carotenoids was reconstructed within Passeriformes, during the Palaeocene Epoch (66–56 Myr), and not at the base of crown-lineage birds.