Predators can reduce herbivory by consuming herbivores (a consumptive effect) and by altering herbivore behavior, life history, physiology or distribution (non-consumptive effects). The non-consumptive, or trait-mediated, effects of predators on prey may have important functions in the dynamics of communities. In a facultative ant-plant mutualism, we investigated whether these non-consumptive effects influenced the host plants of prey. Here, predaceous ants (Forelius pruinosus) consume and disturb a dominant lepidopteran folivore (Bucculatrix thurberiella) of wild cotton plants (Gossypium thurberi). Season-long ant exclusion experiments revealed that ants had a larger proportional effect on damage by B. thurberiella than on caterpillar abundance, a result that suggests ants have a strong non-consumptive effect. Behavioral experiments conducted in two populations over 2 years demonstrated that B. thurberiella caterpillars were substantially less likely to damage wild cotton leaves in the presence of ants due to ant-induced changes in caterpillar behavior. In the absence of ants caterpillars spent more time stationary (potential feeding time) and less time dropping from leaves by a thread of silk than when ants were present. Furthermore, ants altered the spatial distribution of both caterpillars and damage; caterpillars spent relatively more time on the upper surfaces of leaves and caused damage further from the leaf margin in ant exclusion treatments. Both direct encounters with ants and information conveyed when ants walked onto leaves were key events leading to the anti-predator behaviors of caterpillars. This study contributes to a small body of evidence from terrestrial systems demonstrating that the trait-mediated effects of predators can cascade to the host plants of prey.