Wounding is the first event triggering regeneration1–4. However, the molecular basis of wound signalling pathways in plant regeneration is largely unclear. We previously established a method to study de novo root regeneration (DNRR) in Arabidopsis thaliana5,6, which provides a platform for analysing wounding. During DNRR, auxin is biosynthesized after leaf detachment and promotes cell fate transition to form the root primordium5–7. Here, we show that jasmonates (JAs) serve as a wound signal during DNRR. Within 2 h of leaf detachment, JA is produced in leaf explants and activates ETHYLENE RESPONSE FACTOR109 (ERF109). ERF109 upregulates ANTHRANILATE SYNTHASE α1 (ASA1)—a tryptophan biosynthesis gene in the auxin production pathway8–10—dependent on the pre-deposition of SET DOMAIN GROUP8 (SDG8)-mediated histone H3 lysine 36 trimethylation (H3K36me3)11 on the ASA1 locus. After 2 h, ERF109 activity is inhibited by direct interaction with JASMONATE-ZIM-DOMAIN (JAZ) proteins to prevent hypersensitivity to wounding. Our results suggest that a dynamic JA wave cooperates with histone methylation to upregulate a pulse of auxin production and promote DNRR in response to wounding. Using de novo root regeneration from a detached Arabidopsis leaf as a model system, the authors show that jasmonates are a crucial signalling step from wounding to a local auxin response.