Brown planthopper (Nilaparvata lugens) (BPH) is a devastating migratory rice pest in tropical, subtropical, and temperate regions. Insecticide-induced population resurgence is a concern for BPH control. Exposure to low/sublethal concentrations of insecticides has resulted in increased reproduction and fitness as well as insecticide tolerance in many insects. Nitenpyram, a neonicotinoid insecticide, has been frequently used in BPH control. In the present study, the transgenerational hormesis effects in terms of fitness-related traits and insecticide tolerance induced by low concentrations of nitenpyram were reported in both susceptible (S) and field-collected strains (F) of BPH, after exposure to their respective LC20 nitenpyram concentrations for six generations. Our findings stressed that chronic, multigenerational preconditioning of BPHs to LC20 nitenpyram not only increased the biological fitness (in terms of life table parameters and estimated population size), but also primed BPHs to be more tolerate/resistant to insecticides nitenpyram, imidacloprid and cycloxaprid. The upregulation of detoxification (CYP6ER1) and fecundity-related (vitellogenin) genes in both the LC20-preconditioned S and F strains (S-Sub(6) and F-Sub(6)) might contribute to the increased insecticide tolerance and reproduction hormesis. These results support the hypothesis that BPH population outbreaks following multigenerational exposure to low concentrations of nitenpyram in field crops occur through increased reproduction and resistance development. Moreover, based on our results, sulfoxaflor and triflumezopyrim are proposed to be used in rotation with nitenpyram, imidacloprid or cycloxaprid to delay the development of tolerance/resistance in BPHs in paddy fields.