Increased insecticide resistance among insect vectors and arboviruses results in significant economic losses to agricultural production and poses a continuous threat to food safety. To date, many studies have been conducted on how virus-infected host plants indirectly and plant virus directly change the physiological characteristics of insect vectors. However, the relationship between the insecticide resistance of the insect vector and the virulence of the viral pathogen has not received sufficient attention. Here, we investigated the effect of Cucurbit chlorotic yellows virus (CCYV), a plant virus transmitted by whitefly (Bemisia tabaci) in a semi-persistent manner, on the resistance of B. tabaci to the neonicotinoid imidacloprid. We found CCYV enhanced the resistance of B. tabaci to imidacloprid. The CYP6CM1 gene was significantly up-regulated in viruliferous susceptible B. tabaci compared with non-viruliferous B. tabaci after an acquisition access period of 10 d, including its upstream regulators. Silencing the CYP6CM1 gene by RNA interference reduced the ability of B. tabaci to acquire CCYV compared with the control. Additionally, imidacloprid-resistant B. tabaci outperformed sensitive adults in terms of virus transmission ability. These results suggest that CCYV enhances the ability of imidacloprid-sensitive B. tabaci to resist adverse external factors (insecticides). In turn, B. tabaci resistance affects virus transmission. Thus, to a certain extent, the plant virus and insect vector establish a mutually beneficial relationship that facilitates virus transmission.