To understand why avian eggs are so variable in colour and patterning, we investigated contemporary species that provide insights into the evolutionary transitions that occurred during the early radiation of the songbirds. We quantified egg colour and patterning from museum collections of 269 species of Australian passerine and collated it to nest type data (cup or dome nesting species). Using phylogenetically reconstructed trait data, we showed that the ancestral passerine egg was likely to be white, and to have been laid inside a domed nest. Egg colouration and nest type were both phylogenetically clustered, and there was evidence of correlated evolution between the two traits. As nests transitioned from domes to cups, there was an increase in the range of egg colours observed, presumably as a response to additional stressors. Finally, we found that egg colour changes occurred more than twice as frequently in cup nesting species than in dome nesting species. This suggests that cup-nesting species may be using colour as an adaptive trait to compensate for the loss of the protective nest roof.