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<i>Salmonella enterica</i> serovar Typhimurium is a facultative intracellular pathogen that infects humans and animals. Survival and growth in host macrophages represents a crucial step for <i>S</i>. Typhimurium virulence. Many genes that are essential for <i>S</i>. Typhimurium proliferation in macrophages and associated with virulence are highly expressed during the intracellular lifecycle. <i>yaeB</i>, which encodes an RNA methyltransferase, is also upregulated during <i>S</i>. Typhimurium growth in macrophages. However, the involvement of YaeB in <i>S</i>. Typhimurium pathogenicity is still unclear. In this study, we investigated the role of YaeB in <i>S</i>. Typhimurium virulence. Deletion of <i>yaeB</i> significantly impaired <i>S</i>. Typhimurium growth in macrophages and virulence in mice. The effect of <i>yaeB</i> on pathogenicity was related to its activation of <i>pstSCAB</i>, a phosphate (P_i)-specific transport system that is verified here to be important for bacterial replication and virulence. Moreover, qRT-PCR data showed YaeB was induced by the acidic pH inside macrophages, and the acidic pH passed to YeaB through inhibiting global regulator histone-like nucleoid structuring (H-NS) which confirmed in this study can repress the expression of <i>yaeB</i>. Overall, these findings identified a new virulence regulatory network involving <i>yaeB</i> and provided valuable insights to the mechanisms through which acidic pH and low P_i regulate virulence.