Vectors of viruses and other plant pathogens are known to often be attracted by pathogen-infected plants, which promotes pathogen spread. However, few studies have examined how virus-induced changes in plant volatiles mediate such preference. Previous research has demonstrated that tomato plants become more attractive to the whitefly Bemisia tabaci when they are infected by the begomovirus Tomato yellow leaf curl virus (TYLCV). In the current study, we found that the increase in attractiveness is associated with TYLCV-repressed terpenoid synthesis in the virus-infected plants. The observed TYLCV suppression of terpenoid synthesis is similar to the suppression of terpenoid synthesis induced by whitefly infestation. Secondary metabolite analyses and olfactometer experiments with mutant plants revealed that a reduced release of terpenoids through TYLCV-induced suppression of flavonoid synthesis causes B. tabaci females to prefers TYLCV-infected plants over non-infected plants. These results show that TYLCV infection triggers the same changes in odor signaling as caused by B. tabaci infestation, such that both B. tabaci infestation and TYLCV infection increase whitefly aggregation and thereby increase vector acquisition and spread of TYLCV.