AbstractAdaptive radiations have long served as living libraries to study the build‐up of species richness; however, they do not provide good models for radiations that exhibit negligible adaptive disparity. Here, we review work on damselflies to argue that nonadaptive mechanisms were predominant in the radiation of this group and have driven species divergence through sexual selection arising from male–female mating interactions. Three damselfly genera (Calopteryx,EnallagmaandIschnura) are highlighted and the extent of (i) adaptive ecological divergence in niche use and (ii) nonadaptive differentiation in characters associated with reproduction (e.g. sexual morphology and behaviours) was evaluated. We demonstrate that species diversification in the genusCalopteryxis caused by nonadaptive divergence in coloration and behaviour affecting premating isolation, and structural differentiation in reproductive morphology affecting postmating isolation. Similarly, the vast majority of diversification events in the sister generaEnallagmaandIschnuraare entirely driven by differentiation in genital structures used in species recognition. The finding that closely related species can show negligible ecological differences yet are completely reproductively isolated suggests that the evolution of reproductive isolation can be uncoupled from niche‐based divergent natural selection, challenging traditional niche models of species coexistence.