The 90 My-old obligate and mutualistic fig–pollinator wasp system is exploited by parasitic non-pollinating fig wasps that are fig-species specific and oviposit into their hosts from the exterior of the fig which serves as a wasp nursery. Using Ficus racemosa as the study system, we investigated the underlying mechanisms employed by parasitic wasps to locate hidden hosts, where only cues from the exterior surface or from the interior of the fig could guide this search. We also determined the preference of different parasitic wasps for oviposition sites and hosts within the fig. We show, for the first time, that the fig wasp ovipositor is an olfactory sensor that responds to host volatiles and gaseous CO2. This sensor could be used by the parasitic wasps to evaluate ecologically relevant cues for oviposition. Chemical footprints left by previously ovipositing wasps also influenced oviposition choice. We found that physiological factors such as ageing and egg load greatly influenced oviposition behavior. These findings reveal the different ways in which parasitic wasps exploit their hosts but also have bearing on the survival of a plant–pollinator mutualism in such a complex and multiply-parasitized system.