Natural plant populations exhibit genetic variation in defense traits against herbivores. Despite a growing body of evidence for herbivore-mediated selection on plant defenses, we still know little about how genetic variation persists in antiherbivore defense traits. Here we present field and experimental evidence for herbivore-mediated frequency-dependent selection that promotes the maintenance of trichome-producing (hairy) and trichomeless (glabrous) plants of Arabidopsis halleri subsp. gemmifera. First, in a natural population where the specialist leaf beetle Phaedon brassicae was prevalent, hairy plants were damaged less when the frequency of neighboring glabrous plants increased. Furthermore, temporal variation in the frequency of the two plant morphs showed that rarer morphs increased in frequency at the scale of 1-m-diameter patches between survey years. Using a mesocosm experiment, we demonstrated a rare-morph advantage for defense (leaf damage and herbivore abundance) and reproduction (flower and clone production) between hairy and glabrous plants in the presence of P. brassicae. However, this rare-morph advantage was not detected when beetles were absent, with glabrous plants having higher reproduction than hairy plants under these conditions regardless of frequency conditions. These findings highlight the overlooked but potentially critical role of herbivore-mediated apparent interaction in maintaining plant defense polymorphism.