Sexual selection is widely understood through the lens of the peacock’s tail – as the evolutionary driver shaping elaborate courtship displays and signals. Less studied is the influence of sexual selection on cognitive abilities or behaviors that allow individuals to regulate how they use those signals. Prevailing theory suggests, for example, that courting males always present their sexually selected signals at maximum intensity and thus exhibit their capacity to bear the associated signaling costs. Yet many social creatures face shifting competitive contexts that would reward more flexible control over signaling behavior. Humans are an obvious example: we conduct our courtship within complex networks of potential eavesdroppers, many of whom may have an interest in our sexual signaling efforts. I propose that the covert linguistic signals we call flirtation are an adaptive response to the shifting competitive pressures that surround human courtship. I will also discuss experiments with another social class of animals with a sophisticated communication system – songbirds – demonstrating that humans’ flexible signaling is far from unique.