Plants are sessile and have to cope with environmentally induced damage through modification of growth and defense pathways. How tissue regeneration is triggered in such responses and whether this involves stem cell activation is an open question. The stress hormone jasmonate (JA) plays well-established roles in wounding and defense responses. JA also affects growth, which is hitherto interpreted as a trade-off between growth and defense. Here, we describe a molecular network triggered by wound-induced JA that promotes stem cell activation and regeneration. JA regulates organizer cell activity in the root stem cell niche through the RBR-SCR network and stress response protein ERF115. Moreover, JA-induced ERF109 transcription stimulates CYCD6;1 expression, functions upstream of ERF115, and promotes regeneration. Soil penetration and response to nematode herbivory induce and require this JA-mediated regeneration response. Therefore, the JA tissue damage response pathway induces stem cell activation and regeneration and activates growth after environmental stress. Display omitted •The plant RETINOBLASTOMA homolog integrates wound signaling pathways•Jasmonate signaling promotes tissue regeneration•Synergy between jasmonate and auxin signaling in regulating regeneration•Jasmonate-mediated regeneration response is required for abiotic and biotic stresses Stem cell activation and regeneration after tissue damage in Arabidopsis roots is mediated by a jasmonate signaling network.