Plant-emitted volatile organic compounds (VOCs) play fundamental roles in atmospheric chemistry and ecological processes by contributing to aerosol formation and mediating species interactions. Rising temperatures and the associated shifts in vegetation composition have been shown to be the primary drivers of plant VOC emissions in Arctic ecosystems. Although herbivorous insects also strongly alter plant VOC emissions, no studies have addressed the impact of herbivory on plant VOC emissions in the Arctic. Here we show that warming dramatically increases the amount, and alters the blend, of VOCs released in response to herbivory. We observed that a tundra ecosystem subjected to warming, by open-top chambers, for 8 or 18 years showed a fourfold increase in leaf area eaten by insect herbivores. Herbivory by autumnal moth (Epirrita autumnata) larvae, and herbivory-mimicking methyl jasmonate application, on the widespread circumpolar dwarf birch (Betula nana) both substantially increased emissions of terpenoids. The long-term warming treatments and mimicked herbivory caused, on average, a two- and fourfold increase in monoterpene emissions, respectively. When combined, emissions increased 11-fold, revealing a strong synergy between warming and herbivory. The synergistic effect was even more pronounced for homoterpene emissions. These findings suggest that, in the rapidly warming Arctic, insect herbivory may be a primary determinant of VOC emissions during periods of active herbivore feeding.