Animals have encountered novel foods at points throughout history, due to factors such as range expansions and niche shifts driven by competition. One of the first challenges presented by novel foods is how to eat them. Mouthpart morphology is thus critical during the process of host shifts. Developmental plasticity in mouthparts is one potential mechanism that may allow animals to tolerate new foods and eventually to thrive upon them. Here, we investigated the extent to which insect mouthparts from two geographically distant populations can converge in morphology when feeding on common resources. We conducted a common garden/reciprocal transplant experiment using two populations of the cactus bug, Narnia femorata, that differ in mouthpart length. This insect uses straw-like mouthparts (hereafter “beak”) to get through the cactus fruit wall to reach the pulp inside. Our experimental results revealed clear developmental plasticity in beak length. Insects from both populations grew longer beaks when they fed on the cactus fruit with the thicker walls, and they grew shorter beaks when they fed on the cactus fruit with the thinner walls. Thus, insects from distant populations exhibited immediate developmental responses to a new food, and in the predicted directions. These results suggest that some fauna may be able to respond more rapidly than predicted when they encounter novel plants.