The evolution of chemical communication and the origin of pheromones are among the most challenging issues in chemical ecology. Current theory predicts that chemical communication can arise from compounds primarily evolved for non-communicative purposes but experimental evidence showing a gradual evolution of non-informative compounds into cues and true signals is scarce. Here we report that females of the parasitic wasp Leptopilina heterotoma use the defensive compound (-)-iridomyrmecin as a semiochemical cue to avoid interference with con- and heterospecific competitors and as the main component of a species-specific sex pheromone. Although competition avoidance is mediated by (-)-iridomyrmecin alone, several structurally related minor compounds are necessary for reliable mate attraction and recognition. Our findings provide insights into the evolution of insect pheromones by demonstrating that the increasing specificity of chemical information is accompanied by an increasing complexity of the chemical messengers involved and the evolution of the chemosensory adaptations for their exploitation.