Complex interactions within multitrophic communities are fundamental to the evolution of individual species that reside within them. One common outcome of species interactions are fitness trade-offs, where traits adaptive in some circumstances are maladaptive in others. Here, we identify a fitness trade-off between fecundity and survival in the cynipid wasp Callirhytis quercusbatatoides that induces multichambered galls on the stem of its host plant Quercus virginiana. We first quantified this trade-off in natural populations by documenting two relationships: a positive association between the trait gall size and fecundity, as larger galls contain more offspring, and a negative association between gall size and survival, as larger galls are attacked by birds at a higher rate. Next, we performed a field-based experimental evolution study where birds were excluded from the entire canopy of 11 large host trees for five years. As a result of the five-year release from avian predators, we observed a significant shift to larger galls per tree. Overall, our study demonstrates how two opposing forces of selection can generate stabilizing selection on a critical phenotypic trait in wild populations, and how traits can evolve rapidly in the predicted direction when conditions change.