Infection with Helicobacter pylori induces various gastric diseases, including ulceration, gastritis and neoplasia. As H. pylori‐induced cellular mechanisms leading to these disease states are widely unclear, we analysed the phosphoproteome of H. pylori‐infected gastric epithelial cells. Phosphoproteins from infected cells were enriched using affinity columns and analysed by two‐dimensional gel electrophoresis and mass spectrometry. Eleven novel phosphoproteins that showed differentially regulated phosphorylation levels during H. pylori infection were identified. Interestingly, the identified proteins were actin‐binding, transport and folding, RNA/DNA‐binding or cancer‐associated proteins. We analysed functions of one identified H. pylori‐regulated candidate, the vasodilator‐stimulated phosphoprotein (VASP). H. pylori induced VASP phosphorylation at residues Ser157, Ser239 and Thr278, which was enhanced by the bacterial oncogene cytotoxin‐associated gene A. Overexpression of a phosphorylation‐resistant VASP mutant efficiently blocked host cell elongation. We identified cGMP‐dependent protein kinase G‐mediated Ser239 and Thr278 phosphorylation of VASP as a crucial event in H. pylori‐dependent host cell elongation. These results suggest that phosphorylated VASP could be a novel target candidate for therapeutic intervention in H. pylori‐related gastric diseases.