A major challenge in evolutionary biology concerns how genetic and phenotypic variation is created and maintained. In this study, we investigated the origin(s) and evolutionary patterns of the female-limited colour polymorphism in Ischnura. This involves the presence of one to three colour morphs: one androchrome morph with coloration that resembles that of the male, and two gynochrome morphs (infuscans and aurantiaca) with a female-specific coloration. We documented the colour of 44 and mating system of 36 of the 76 species within Ischnura to investigate the ancestral state of both traits and the correlated evolution and to infer directionality of trait-state transitions. The ancestral state reconstructions suggest that the most recent common ancestor of the ischnuran damselflies was most likely polymorphic and polyandrous. Our results give some support to the evolutionary correlation between female-limited colour polymorphism and mating system in Ischnura. That correlation is consistent with the idea that sexual selection through sexual conflict over the frequency of matings has selected for polymorphic females to reduce the overall intensity of male mating harassment, and our finding that the same phenotypic morphs have evolved multiple times (convergent evolution) suggests that several species in this genus might be experiencing similar selective pressures.