Every year, rice planthoppers (main brown planthopper, BPH, Nilaparvata lugens Stål), one of the most important pests in rice production, cause huge yield losses worldwide. The identification of resistance genes and exploration of insect resistance mechanisms are some of the most fundamental and effective methods to manage the pest. Here, the aspartic protease (AP) gene OsAP79 was transcriptionally expressed in all organs tested, particularly in the roots at the adult stage. The knockout of OsAP79 impaired rice resistance to BPH, whereas overexpression (OE) of OsAP79 improved rice resistance by increasing plant survival rates, and reducing BPH weight gain and honeydew excretion. Observation of the transverse section of rice shoots indicated that OE lines of OsAP79 can significantly enhance sclerenchyma layer thickness. Meanwhile, a significantly longer or shorter root was detected in the knockout or OE lines, respectively, which was positively correlated with the indole acetic acid (IAA) content. Hormone measurement and metabolomic analysis suggested that IAA biosynthesis, the citric acid cycle, and glycolysis biosynthesis contributed greatly the OsAP79-induced resistance of rice against BPH. Collectively, OsAP79 was continuously induced to express and enhance BPH resistance by reducing the IAA content, which restricts root growth and increases shoot sclerenchyma layer thickness. This study demonstrates the previously unappreciated importance of the AP gene in rice for combating piercing-sucking insect herbivores.