Many herbivorous insects rely on plant volatiles to locate their host plants. Vector-borne viral infections induce changes in plant volatiles, which render infected plants more attractive to insect vectors. However, the detailed mechanisms underlying the olfactory responses of insect vectors induced by the volatiles produced by virus-infected plants are poorly understood. Here, we show that volatiles emitted by pepper (Capsicum annuum) plants infected with tomato zonate spot virus (TZSV), particularly the volatilecis-3-hexenal, which is recognized by chemosensory protein 1 of the thripsFrankliniella intonsa(FintCSP1), are more attractive toF.intonsathan the volatiles emitted by non-infected pepper plants. FintCSP1 is highly abundant in the antenna ofF.intonsa. Silencing ofFintCSP1significantly decreased electroantennogram responses ofF.intonsaantennae tocis-3-hexenal and impaired thrips’ responses to TZSV-infected pepper plants andcis-3-hexenal, as assessed using a Y-tube olfactometer. Three-dimensional model predictions indicated that FintCSP1 consists of seven α-helixes and two disulfide bridges. Molecular docking analysis suggested thatcis-3-hexenal is positioned deep inside the binding pocket of FintCSP1 and binds to residues of the protein. We combined site-directed mutagenesis and fluorescence binding assays and identified three hydrophilic residues, Lys26, Thr28, and Glu67, of FintCSP1 as being critical forcis-3-hexenal binding. Furthermore, CSP ofF.occidentalis(FoccCSP) is also a key olfactory protein involved in modulating the behaviour ofF.occidentalisto TZSV-infected pepper. This study revealed the specific binding characteristics of CSPs tocis-3-hexenal and confirmed the general hypothesis that virus infections induce changes in host volatiles, which can be recognized by the olfactory proteins of the insect vector to enhance vector attraction and this may facilitate viral spread and transmission.