Background/Question/Methods Mutualisms are interspecific interactions in which both players benefit. Explaining their maintenance is problematic, because cheaters should outcompete cooperative conspecifics leading to mutualism instability. A well-known mutualism involves monoecious figs (Ficus) pollinated by host-specific wasps (Agaonidae), whose larvae gall ovules in their ‘fruits’ (syconia). Female pollinating wasps enter receptive syconia and oviposit directly into Ficus ovules. Across Ficus species there is a widely documented segregation of pollinator galls in inner ovules, and seeds in outer ovules, near the fig wall. This pattern suggests that wasps avoid, or are prevented from ovipositing into, outer ovules, which safeguards seed production. However, the mechanisms preventing wasps from exploiting outer ovules remain unknown. Recent optimal foraging models predict that wasps should specialise on laying eggs in inner ovules, ignoring outer ovules, if their offspring gain much higher fitness when they develop in inner ovules. We conducted studies of Ficus rubiginosa at six field sites in Australia to test whether wasp offspring in inner ovules have higher survival or reproductive success. We collected and dissected ripe syconia to assess risk of parasitism and offspring size (fecundity) in inner and outer ovules. We also manipulated syconia to test for effects of ovule position on offspring mating success and emergence.Results/Conclusions We found that offspring in outer ovules are highly vulnerable to attack by parasitic wasps that oviposit from outside the syconium. Parasitism risk decreases from 80% in outer flowers to 0% in the innermost flowers. Inner ovules thus provide enemy-free space for pollinator offspring. In addition, surviving wasps in outer ovules also have reduced chances of mating and emerging from their galls. We suggest that the resulting spatial gradient in offspring fitness contributes to selection on egg-laying pollinators to avoid outer ovules, and by forcing wasps to focus on an inner subset of ovules, reduces their overall seed galling rates. These results emphasise how third parties can play crucial roles in the dynamics of mutualisms, which may often be embedded in a wider network of species interactions.