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<i>Cronobacter sakazakii</i>, an emerging foodborne pathogen that was isolated primarily from powdered infant formula, poses an important issue in food safety due to its high stress tolerance and pathogenicity. The Hpr (encoded by <i>ptsH</i> gene) has been shown to regulate carbon metabolism as well as stress response and virulence. However, the functional properties of <i>ptsH</i> in <i>C. sakzakii</i> have not been investigated. In this study, we clarified the role of <i>ptsH</i> in the <i>C. sakzakii</i> stress response and virulence, and explored its possible regulatory mechanism by RNA-seq. Compared with wild-type, the Δ<i>ptsH</i> mutant showed a slower growth rate in the log phase but no difference in the stationary phase. Moreover, the resistance to heat stress (65 °C, 55 °C), simulated gastric fluid (pH = 2.5), biofilm formation and adhesion to HT-29 cells of Δ<i>ptsH</i> mutant were significantly decreased, whereas the oxidative resistance (1, 5, 10 mM H₂O₂), osmotic resistance (10%, 15%, 20% NaCl), and superoxide dismutase activity were enhanced. Finally, RNA-seq analysis revealed the sulfur metabolism pathway is significantly upregulated in the Δ<i>ptsH</i> mutant, but the bacterial secretion system pathway is dramatically downregulated. The qRT-PCR assay further demonstrated that the Δ<i>ptsH</i> mutant has elevated levels of genes that are related to oxidative and osmotic stress (<i>sodA</i>, <i>rpoS</i>, <i>cpxA</i>/<i>R</i>, <i>osmY</i>). This study provides a great understanding of the role of <i>ptsH</i> in diverse stress responses and virulence in <i>C. sakazakii</i>, and it contributes to our understanding of the genetic determinant of stress resistance and pathogenicity of this important foodborne pathogen.