This study demonstrates that the ericoid mycorrhizal (ERM) fungus RM2 can colonize the non-ericaceous host Malus robusta as a functional endophyte, enhancing drought resilience through an active avoidance strategy. Under drought, inoculation was associated with qualitative changes in root growth patterns, and inoculated seedlings showed a more extensive and branched root appearance compared with non-inoculated controls. This morphological tendency was accompanied by a distinctive physiological state of oxidative priming, characterized by elevated H₂O₂ as a signaling molecule, reduced antioxidant enzyme activity, and a marked shift toward proline-mediated osmotic adjustment. Transcriptomic analysis suggested a molecular basis for these responses: endophytic colonization reprogrammed auxin and brassinosteroid signaling, including the repression of auxin inactivation (GH3) and activation of genes involved in auxin transport (AUX1) and cell wall loosening (TCH4), which is consistent with sustained root growth under drought. Our findings indicate that ERM fungi can transcend traditional host barriers and improve drought performance via integrated oxidative signaling and hormonal regulation, highlighting their potential as cultivable biostimulants for sustainable horticulture.