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Social insect reproductives and non‐reproductives represent ideal models with which to understand the expression and regulation of alternative phenotypes. Most research in this area has focused on the developmental regulation of reproductive phenotypes in obligately social taxa such as honey bees, while relatively few studies have addressed the molecular correlates of reproductive differentiation in species in which the division of reproductive labour is established only in plastic dominance hierarchies. To address this knowledge gap, we generate the first genome for any stenogastrine wasp and analyse brain transcriptomic data for non‐reproductives and reproductives of the facultatively social species Liostenogaster flavolineata, a representative of one of the simplest forms of social living. By experimentally manipulating the reproductive 'queues' exhibited by social colonies of this species, we show that reproductive division of labour in this species is associated with transcriptomic signatures that are more subtle and variable than those observed in social taxa in which colony living has become obligate; that variation in gene expression among non‐reproductives reflects their investment into foraging effort more than their social rank; and that genes associated with reproductive division of labour overlap to some extent with those underlying division of labour in the separate polistine origin of wasp sociality but only explain a small portion of overall variation in this trait. These results indicate that broad patterns of within‐colony transcriptomic differentiation in this species are similar to those in Polistinae but offer little support for the existence of a strongly conserved 'toolkit' for sociality. [ABSTRACT FROM AUTHOR]