All aphid species studied so far share the same sex pheromone components, nepetalactol and nepetalactone. Variation by different enantiomers and blends of the two components released by different aphid species are limited and can only partially explain species-specific attraction of males to females. While some host-plant odours are known to enhance specific attraction of aphid species, herbivore-induced plant volatiles that synergise attractiveness to the sex pheromone are unknown. Here, we demonstrate that for the host-alternating rosy apple aphid (Dysaphis plantaginea (Passerini)) specificity of attraction of males to females is triggered by female-induced tree odours in combination with a 1:8 ratio of (4aS,7S,7aR)-nepetalactone and (1R,4aS,7S,7aR)-nepetalactol. Female aphid infestation induces increased release of four esters (hexyl butyrate, (E)-2-hexenyl butyrate, (Z)-3-hexenyl 3-methylbutyrate and hexyl 2-methylbutyrate) from apple leaves. Two different combinations of three esters applied in a 1:1:1 ratio increase the number of male D. plantaginea and decrease the number of other aphid species caught in water traps in the presence of the pheromone components. The ester blend alone was not attractive. Combination of the pheromone blend with each single ester was not increasing attraction of male D. plantaginea. The demonstration that sexual aphid species use herbivore-induced plant volatiles as a species-specific attractant for mate finding adds a new dimension to our understanding of insect species using or manipulating chemical cues of host plants for orientation.