Tomato yellow leaf curl virus (TYLCV), a devastating pathogen of tomato crops, is vectored by the whitefly Bemisia tabaci, yet the mechanisms underlying TYLVC epidemics are poorly understood. We found that TYLCV triggers the up-regulation of two β-myrcene biosynthesis genes in tomato, leading to the attraction of nonviruliferous B. tabaci. We also identified BtMEDOR6 as a key whitefly olfactory receptor of β-myrcene involved in the distinct preference of B. tabaci MED for TYLCV-infected plants. TYLCV inhibits the expression of BtMEDOR6, canceling this preference and thereby facilitating TYLCV transmission to uninfected plants. Greenhouse experiments corroborated the role of β-myrcene in whitefly attraction. These findings reveal a sophisticated viral strategy whereby TYLCV modulates both host plant attractiveness and vector olfactory perception to enhance its spread.