Abstract Abiotic stresses significantly impact agricultural productivity and food security. Innovative strategies, including the use of plant‐derived compounds and plant growth‐promoting rhizobacteria (PGPR), are necessary to enhance plant resilience. This study delved into how Bacillus zanthoxyli HS1 ( Bza HS1) and Bza HS1‐derived volatile organic compounds (VOC) conferred systemic tolerance against salt and heat stresses in cabbage and cucumber plants. Direct application of a Bza HS1 strain or exposure of Bza HS1‐derived VOC to cabbage and cucumber plants promoted seedling growth under stressed conditions. This induced systemic tolerance was associated with increased mRNA expression and enzymatic activities of superoxide dismutase (EC 1.15.1.1), catalase (EC 1.11.1.6), or ascorbate peroxidase (EC 1.11.1.1), leading to a reduction in oxidative stress in cabbage and cucumber plants. Plants co‐cultured with Bza HS1 and exposed to Bza HS1‐derived VOC triggered the accumulation of callose and minimized stomatal opening in response to high salt and temperature stresses, respectively. In contrast, exogenous treatment of azelaic acid, a well‐characterized plant defense primer, had no significant impact on the seedling growth of cabbage and cucumber plants grown under abiotic stress conditions. Taken together, Bza HS1 and its VOC show potential for enhancing plant tolerance responses to salt and heat stresses through modulation of osmotic stress‐regulatory networks.