Herbivore populations are regulated by plant defenses and natural enemies. While plant defense can suppress herbivore populations, these defenses adversely affect natural enemies thereby releasing herbivores from top-down control. Over their lifespans, herbivores and their natural enemies may experience substantial variation in plant defense. Defense variability can suppress the growth of herbivores, but the impacts of defense variability on natural enemies and top-down control of herbivores are unknown. We independently manipulated the mean and variation of a plant toxin experienced by individual Trichoplusia ni caterpillars and its parasitoid Copidosoma floridanum. Increases in the mean toxin concentration, but not its variance, experienced by individual T. ni and C. floridanum decreased the fitness of C. floridanum, whereas both mean and variance impacted T. ni fitness. Thus, increased defense variability for individual herbivores suppressed herbivore fitness with no perceptible cost to top-down control. However, impacts of variability depend heavily on scale of variability.