Flavonoids are secondary metabolites that help plants resist insect attack, but pest insects have evolved enzymes that reduce the toxicity of these secondary metabolites. We studied the response of the grasshopper Oedaleus asiaticus Bey-Bienko fed different concentrations of quercetin, a representative flavonoid. Oedaleus asiaticus growth (survival rate and growth rate) was significantly reduced at high quercetin concentrations. Reactive oxygen species (ROS) increased significantly in response to the diet stress associated with high quercetin concentrations. Gene expression and protein phosphorylation level of the IGF→FOXO cascade related to the stress response in the O. asiaticus insulin-like signaling pathway (ILP) were also reduced. Multiple protective enzyme activities were regulated by FOXO. Mixed-function oxidase (MFO), superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT), were all significantly increased with exposure to high quercetin concentrations. Quercetin negatively regulated the ILP pathway, and was detrimental to O. asiaticus growth and survival, as more energy was required for detoxification. This study showed how flavonoids impact on O. asiaticus biochemical pathways, physiology, and development. Flavonoids offer a new option for the development of biological pesticides for application to grasshopper biological control.