Summary The production of defensive metabolites in plants can be induced by signaling chemicals released by neighboring plants. Induction is mainly known from volatile aboveground signals, with belowground signals and their underlying mechanisms largely unknown. We demonstrate that (−)‐loliolide triggers defensive metabolite responses to competitors, herbivores, and pathogens in seven plant species. We further explore the transcriptional responses of defensive pathways to verify the signaling role of (−)‐loliolide in wheat and rice models with well‐known defensive metabolites and gene systems. In response to biotic and abiotic stressors, (−)‐loliolide is produced and secreted by roots. This, in turn, induces the production of defensive compounds including phenolic acids, flavonoids, terpenoids, alkaloids, benzoxazinoids, and cyanogenic glycosides, regardless of plant species. (−)‐Loliolide also triggers the expression of defense‐related genes, accompanied by an increase in the concentration of jasmonic acid and hydrogen peroxide (H2O2). Transcriptome profiling and inhibitor incubation indicate that (−)‐loliolide‐induced defense responses are regulated through pathways mediated by jasmonic acid, H2O2, and Ca 2+. These findings argue that (−)‐loliolide functions as a common belowground signal mediating chemical defense in plants. Such perception‐dependent plant chemical defenses will yield critical insights into belowground signaling interactions. See also the Commentary on this article by Frost, 238: 1749–1751.