The bacterium Helicobacter pylori tightly regulates the host immune response to dampen inflammation and promote persistence. Excessive inflammatory responses to the bacterium, however, promote gastric carcinogenesis. Several H. pylori proteins have been associated with an increased risk of gastric cancer. One of these proteins, tumour necrosis factor-a-inducing protein (Tipa), when produced in its recombinant form was reported to traffic to the host cell nucleus, leading to tumour necrosis factor (TNF) gene expression and carcinogenic effects. Although Tipa is secreted by the bacterium, we showed in proteomic studies that it is also released by bacterial extracellular vesicles (BEVs); these membrane “blebs” are highly efficient at entering and subverting host cell functions. We hypothesised that H. pylori BEVs carry Tipa to the nucleus, resulting in perturbed nuclear processes that promote carcinogenesis. To address this hypothesis, we generated H. pylori tipA mutants and complemented tipA/tipA+ strains. By immunoblotting, we confirmed that H. pylori BEVs harbour Tipa. In addition, the quantity of Tipa secreted into culture supernatants varied between H. pylori strains, but was not associated with disease outcome. Gastric epithelial cells (AGS) were treated with H. pylori OMVs or recombinant Tipa (rTipa). By immunoblotting and confocal microscopy, we showed that BEV-associated Tipa is present within the cytoplasm at 4 hours post-treatment and accumulates in the nuclear compartment by 18 hours. We then tested the ability of Tipa to induce pro-inflammatory signalling in AGS and THP-1-derived macrophages. Consistent with previous work, rTipa induced TNF production in THP-1 cells. Conversely, BEVs from tipA bacteria induced significantly less TNF than those from wild-type (WT) or tipA/tipA+ bacteria (p < 0.0001), as well as significantly less IL-8 production in AGS (p = 0.036) and THP-1 cells (p = 0.018). Taken together, we propose that BEV-associated Tipa may dampen pro-inflammatory responses but promote carcinogenesis in H. pylori infection.