The evolution of the nonapeptide system in vertebrates is characterised by gene duplication events that gave rise to a separation of behavioural functions between two signalling pathways, oxytocin and vasotocin. This is particularly marked in fish, which present the greatest diversity in social behaviour among vertebrates. Notably, the conservation of nonapeptide activity across homologous brain areas offers an opportunity to identify the mechanisms underlying social evolution in this group of animals. Here we describe the evolutionary history of the nonapeptide ligands and their receptors in fish and discuss up-to-date evidence of their role in social phenotypes. We present evidence for a broad implication of nonapeptides in the variation in social behaviour both across and within species. Much of the evidence is derived from pharmacological manipulations, but recently genetic tools have also been developed for model organisms, such as zebrafish and medaka. The time is now right to expand genetic approaches from model organisms in more ecologically relevant models in the field.