In population ecology, dispersal plays a fundamental role, but is potentially costly. Traditionally, studies of phenotypic trade-offs involving dispersal focus on resource allocation differences between flight and reproduction. However, investments in dispersal may also result in reduced allocation to other "third-party traits" (e.g. compensatory feeding) that are not directly associated with reproduction. Such traits remain largely uninvestigated for any phytophagous insect despite their importance for performance and survival. Using two wing-dimorphic, phloem-feeding planthoppers, Prokelisia dolus and Prokelisia marginata that differ dramatically in dispersal abilities, we sought evidence for a trade-off between investments in dispersal (flight apparatus) and ingestion capability (allocation to the esophageal musculature governing ingestion). Dispersal allows species to meet nutrient demands by moving to higher-quality resources. In contrast, enhanced investment in esophageal musculature increases ingestion capacity and allows phloem feeders to compensate for deteriorating plant nutrition on site. Our objectives were to compare differences in flight and feeding investment between P. dolus and P. marginata and between the wing forms of both species, and to compare ingestion capacity between the two species and wing forms. Morphometric and gravimetric measures of investment in flight versus feeding indicate that the sedentary P. dolus allocates more muscle mass to feeding whereas P. marginata invests more heavily in flight. Likewise, brachypters invest more in feeding and less in flight than macropters. The greater esophageal investment in P. dolus is associated with enhanced ingestion capacity compared to P. marginata. As a consequence, P. dolus is better equipped to meet on-site nutrient demands when faced with deteriorating plant quality than P. marginata, which must migrate elsewhere to do so. Notably, such third-party trade-offs place constraints on how insect herbivores cope with changing resources and set the stage for fundamental differences in population dynamics.