Among the many ways arthropod pests may signal their whereabouts to natural enemies, the release of specific volatiles by either pests themselves or their infested host plants may represent some of the most valuable cues that dictate biocontrol agent host-attraction, trophic impact and host-specificity. In this study, we sought to elucidate how plant and insect host-specific volatiles mediate attraction of pteromalid wasp, Jaliscoa hunteri to immature pepper weevil, Anthonomus eugenii, an economically important and challenging-to-control pest of cultivated Capsicum sp. pepper crops across North America. To begin, we used an air-entrainment system to collect volatiles released by whole pepper plants infested or not by either egg, L1 or L3 stages of pepper weevil and in the presence or absence of parental adults. The chemical analysis of sample volatiles from pepper plants infested or not with A. eugenii larvae were then compared, and among these, five compounds were identified that had their emission increased from 1.5 to 8.1 times relative to the blend of volatiles emitted by undamaged pepper plants including: linalool, 1-hexanol, 4,8-dimethylnona-1,3,7-triene (DMNT), methyl salicylate, and 4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT). We next conducted Y olfactometer bioassays to compare the attractive potential of volatiles emitted by pepper fruit, infested or not by L1 or L3 immature pepper weevil, as well as by the alternative J. hunteri-rearing host, L3 or L4 immature Callosobruchus maculatus as they developed within infested chickpeas. Olfactometer bioassays showed that J. hunteri females preferred and consistently oriented towards the volatiles derived from pepper fruit infested by both larval stages of pepper weevil compared to the odour of undamaged pepper fruit. The females of J. hunteri also preferred for the odour emitted by chickpeas infested with C. maculatus compared to air. Ultimately this work highlights the considerable value of studying the composition of volatile headspace captures for pest-infested fruit and complimentary Y-tube assays for measuring or even improving the attraction potential of natural enemies to economically or ecologically important host species.