Herbivore communities are shaped by indirect plant-mediated interactions whose outcomes are strongly dependent on the sequence of herbivore arrival. However, the mechanisms underlying sequence specificity are poorly understood. We examined the mechanisms that govern sequence-specific effects of the interaction between two specialist maize herbivores, the leaf feeder Spodoptera frugiperda and the root feeder Diabrotica virgifera virgifera. In the field, S. frugiperda reduces D. v. virgifera abundance, but only when it arrives on the plant first. In behavioral experiments, D. v. virgifera larvae continued feeding on plants that they had infested before leaf infestation, but refused to initiate feeding on plants that were infested by S. frugiperda before their arrival. Changes in root-emitted volatiles were sufficient to elicit this sequence-specific behavior. Root volatile and headspace mixing experiments showed that early-arriving D. v. virgifera larvae suppressed S. frugiperda-induced volatile repellents, which led to the maintenance of host attractiveness to D. v. virgifera. Our study provides a physiological and behavioral mechanism for sequence specificity in plant-mediated interactions and suggests that physiological canalization of behaviorally active metabolites can drive sequence specificity and result in strongly diverging herbivore distribution patterns.