Carotenoid-based colours are recognized as having an important signalling function, yet the nature of the mechanisms that maintain their honesty is not well understood. By combining a carotenoid-feeding experiment with a quantitative genetic experiment in a wild population of blue tits (Parus caeruleus), we were able to test predictions that differentiate between proposed mechanisms. If variation in carotenoid ingestion underlies variation in carotenoid-based colour expression, then carotenoid-supplemented birds should have reduced variance in colour. In this study, carotenoid supplementation produced a small but significant change in plumage colouration, but no significant change in variation. These results suggest that variation in carotenoid acquisition is not an important source of variation for this colour trait, and that variation in post-ingestion processes are likely to be more important. The low heritability of this colour trait suggests environmental factors are likely to underlie the majority of variation in these processes.