Despite broad interest and recent experimentation, there is no single ecological model accounting for the adaptive significance of the diversity of avian eggshell colouration. The often blue-green eggs of Turdus thrushes are a charismatic example of this, having long captured cultural and scientific attention. Although the biology and evolutionary history of “true” thrushes is well understood, little is known about correlated evolution between shifts in habitat and eggshell pigmentation, and how these shifts map with Turdus biogeography. We applied phylogenetic comparative methods to assess the evolutionary timing of divergence and variation of life history traits and eggshell colouration and maculation presence in the genus. We found that eggshell colour diversified independently on several occasions in the past 11 million years, with much of the variation occurring within the last 4 million years. The majority of Turdus species lay blue-green eggs and also tend to be sedentary and forest-dwelling. Diet generalist species and species which have transitioned to a forest habitat are more likely to lay white eggs (10% of studied species). In turn, lineages in any habitat were more likely to transition to blue-green eggs. We found that variation in egg colour is increased in some clades, of which two lineages radiated in South America and the East Palearctic, in the past 2–4 million years. These findings provide support for the hypothesis that white eggs are more conspicuous to predators in open environments and that multiple, non-mutually exclusive constraints operate on the adaptive function of avian eggshell colour.