Animals must locate prey and mates in noisy sensory environments. Species that rely on visual cues, and which are prey of visual predators, consequently face trade-offs. Additionally, within species, sexual conflict over mating may impose pressures to avoid both predators and mates. Many studies have attempted to explain female-specific polymorphisms in damselflies, but without considering their actual conspicuousness under natural conditions. Using models of colour perception for damselflies and birds, we assessed the detectability of female coloration to conspecific males and potential predators. Alternative colour morphs reduce female apparency either through signal similarity with conspecific males (i.e. mimicry) or by matching the noise of the visual background. The colours of male-mimicking andromorphs that reduce their apparency among groups of males at breeding sites render them highly detectable to males as well as visual predators in offshore vegetation, where females occur when not reproducing. By presenting tethered female damselflies to free-flying males amidst vegetation, we demonstrated that, among flying females, males were able to detect andromorphs more easily than the more cryptic heteromorphs. Thus, when male density is low, cryptic heteromorphs may experience less harassment than andromorphs, suggesting a scenario of disruptive selection on female coloration driven by males as well as predators. Greater attention is warranted not only to the predation risks of female signals, but also to the effect of variation in the visual environments on encounters between males and unreceptive females.