1. Environmental change has the potential to influence trophic interactions by altering the defensive phenotype of prey. 2. Here, we examine the effects of a pervasive environmental change driver, elevated atmospheric concentrations of CO2 (eCO2), on toxin sequestration and flight morphology of a specialist herbivore. 3. We fed monarch butterfly larvae, Danaus plexippus, foliage from four milkweed, Asclepias, species of varying chemical defense profiles grown under either ambient or eCO2. We also infected a subset of these herbivores with a protozoan parasite, Ophryocystis elektroscirrha, to understand how infection and environmental change combine to alter herbivore defenses. We measured changes in phytochemistry induced by eCO2 and assessed cardenolide, toxic steroid, sequestration and wing morphology of butterflies. 4. Monarchs compensated for lower plant cardenolide concentrations under eCO2 by increasing cardenolide sequestration rate, maintaining similar cardenolide composition and concentrations in their wings under both CO2 treatments. We suggest that these increases in sequestration rate are a byproduct of compensatory feeding aimed at maintaining a nutritional target in response to declining dietary quality. 5. Monarch wings were more suitable for sustained flight (more elongated) when reared on plants grown under eCO2 or when reared on A. syriaca or A. incarnata rather than on A. curassavica or A. speciosa. Parasite infection engendered wings less suitable for sustained flight (wings became rounder) on three of four milkweed species. Wing loading (associated with powered flight) was higher on A. syriaca than on other milkweeds, whereas wing density was lower on A. curassavica. Monarchs that fed on high cardenolide milkweed developed rounder, thinner wings, which are less efficient at gliding flight. 6. Ingesting foliage from milkweed high in cardenolides may provide protection from enemies through sequestration yet come at a cost to monarchs manifested as lower quality flight phenotypes: rounder, thinner wings with lower wing loading values. 7. Small changes in morphology may have important consequences for enemy evasion and migration success in many animals. Energetic costs associated with alterations in defense and morphology may, therefore, have important consequences for trophic interactions in a changing world.