The evolution of bird plumage colouration may be explained by a wide range of selective pressures, including both defensive and advertising needs. However, the relationship between plumage colouration and body size has never been investigated in detail. Here we hypothesize that body size represents a constraint for the evolution of plumage colour heterogeneity because the relative number of body feathers was suggested to increase as body size decreases, and in the case of carotenoid-based colourations because the concentrations of circulating carotenoids decrease with increasing body size. Here we test these predictions on a dataset comprising measurements of male plumage colour heterogeneity using a model of avian visual perception in 111 species from 55 families of birds. A test of the correlation between number of feathers and body size in 92 species of birds showed a positive, instead of negative as previously suggested, association between these variables. As predicted, there was a negative relationship between plumage colour heterogeneity (measured as colour span, a measure of the contrast among colour patches) and body size after controlling for the effects of phylogeny, sexual dichromatism, colour vision type and habitat, and we suggest that the negative allometry shown by carotenoid levels may be the mechanism responsible for this negative relationship. Plumage colour heterogeneity was lower in species inhabiting open environments than in more vegetated habitats. Our results offer a general explanation for interspecific variation in bird colour heterogeneity through an association with body size.