Phenotypic plasticity, where a single genome can give rise to different phenotypes, underlies many remarkable features of the natural world and occurs in a wide range of organisms. Understanding the transcriptional differences that underlie plastic phenotypes remains a major unsolved problem in biology. In many ants, females can develop into either queens or workers, two phenotypes with different morphology, behaviour and longevity. In comparison with workers, queens are larger, more fecund and longer lived. Here, we study gene expression differences between queens and workers in the ant Lasius niger. The analysis of age- and tissue-specific RNA sequencing showed that patterns of caste-biased gene expression vary considerably between ages and tissues. Expression was more tightly linked to age than caste despite the important morphological and behavioural differences between queens and workers. Our data allowed us to identify genes that are consistently biased across biological contexts. Caste-biased genes showed faster rates of molecular evolution, lower levels of DNA methylation and greater variability in expression than unbiased genes. Our results indicate that a substantial proportion of caste-biased expression is ephemeral and that taking account of age and tissue is critical to understanding the transcriptomic basis of plastic phenotypes. By contrast, the biological context of expression bias did not broadly affect methylation or the rate of evolution. The faster rate of evolution and greater variability of expression of caste-biased genes indicate that caste-biased genes evolve from loosely regulated genes that can be co-opted for caste-specific tasks because of the lax control over their expression.