Avian brood parasites lay their eggs in other birds' nests and impose considerable fitness costs on their hosts. Historically and scientifically, the best studied example of circumventing host defences is the mimicry of host eggshell colour by the common cuckoo (Cuculus canorus). Yet the chemical basis of eggshell colour similarity, which impacts hosts' tolerance towards parasitic eggs, remains unknown. We tested the alternative scenarios that (i) cuckoos replicate host egg pigment chemistry, or (ii) cuckoos use alternative mechanisms to produce a similar perceptual effect to mimic host egg appearance. In parallel with patterns of similarity in avian-perceived colour mimicry, the concentrations of the two key eggshell pigments, biliverdin and protoporphyrin, were most similar between the cuckoo host-races and their respective hosts. Thus, the chemical basis of avian host-parasite egg colour mimicry is evolutionarily conserved, but also intraspecifically flexible. These analyses of pigment composition reveal a novel proximate dimension of coevolutionary interactions between avian brood parasites and hosts, and imply that alternative phenotypes may arise by the modifications of already existing biochemical and physiological mechanisms and pathways.