1. Maternally inherited bacterial symbionts are present in many, if not most, insect species. While there is rapidly accumulating evidence that facultative, heritable symbionts often protect insect hosts from natural enemies, there have been few clear examples where facultative symbionts mediate herbivore–plant interactions. 2. The phloem-feeding whitefly, Bemisia tabaci, is a major agricultural pest that frequently harbours facultative symbionts, including Hamiltonella defensa. While H. defensa and other facultative symbionts have been shown to improve whitefly performance on particular food plants, no direct and specific roles for symbiont-mediated interactions with food plants have been identified. 3. Here, we conducted a series of assays to determine whether infection with H. defensa improved whitefly performance on tomato (Solanum lycopersicum) and whether this benefit was associated with symbiont effects on induced plant defences. Finally, we tested whether impacts on induced defences involved in the modulation of a salivary factor. 4. The downregulation of plant defences was associated with increased whitefly fecundity and survival. Feeding by H. defensa-infected whiteflies suppressed JA and JA-related anti-herbivore-induced defences in tomato relative to uninfected controls. That saliva-only treatments of damaged tomato leaves from H. defensa-infected whiteflies suppressed induced plant defences compared to saliva from uninfected controls, suggesting that elicitors in saliva were responsible. Characterization of the putative salivary factor(s) revealed they are likely small (< 3-kDa) and nonproteinaceous. 5. Interestingly, suppression of defences was not observed in SA-deficient NahG plants, indicating that suppression of JA-regulated defences depends on the SA signalling pathway. This finding reveals an intriguing example of the crosstalk between SA and JA signalling pathways and suggests that infection with facultative symbionts can result in the manipulation of induced plant defences to the benefit of the insect host and heritable symbiont. 6. Our results show that the bacterial symbiont H. defensa mediates whitefly–plant interactions by suppressing induced plant defences in tomato. This finding is among the first showing a direct role for facultative symbionts in mediating plant–herbivore interactions and demonstrates a novel tactic for insect herbivores to circumvent plant defences. Symbiont-mediated suppression of plant defences may enhance the deleterious effects of insect pests feeding on important crops.