Ionotropic receptors (IRs) play a central role in detecting chemosensory information from the environment and guiding insect behaviors and are potential target genes for pest control.Empoasca onukiiMatsuda is a major pest of the tea plantCamellia sinensis(L.) O. Ktze, and seriously influences tea yields and quality. In this study, the ionotropic receptor geneEonuIR25ainE. onukiiwas cloned, and the expression pattern ofEonuIR25awas detected in various tissues. Behavioral responses ofE. onukiito volatile compounds emitted by tea plants were determined using olfactometer bioassay and field trials. To further explore the function ofEonuIR25ain olfactory recognition of compounds, RNA interference (RNAi) ofEonuIR25awas carried out by ingestion of in vitro synthesized dsRNAs. The coding sequence (CDS) length ofEonuIR25awas 1266 bp and it encoded a 48.87 kD protein.EonuIR25awas enriched in the antennae ofE. onukii.E. onukiiwas more significantly attracted by 1-phenylethanol at a concentration of 100 µL/mL. Feeding with dsEonuIR25a significantly downregulated the expression level ofEonuIR25a, after 3 h of treatment, which disturbed the behavioral responses ofE. onukiito 1-phenylethanol at a concentration of 100 µL/mL. The response rate ofE. onukiito 1-phenylethanol was significantly decreased after dsEonuIR25a treatment for 12 h. In summary, the ionotropic receptor geneEonuIR25awas highly expressed in the antennae ofE. onukiiand was involved in olfactory recognition of the tea plant volatile 1-phenylethanol. The present study may help us to use the ionotropic receptor gene as a target for the behavioral manipulation ofE. onukiiin the future.