Staphylococcus aureus, a Gram‐positive pathogen, invades cells mainly in an integrin‐dependent manner. As the activity or conformation of several integrin‐associated proteins can be regulated by phosphatidylinositol‐4,5‐bisphosphate (PI‐4,5‐P2), we investigated the roles of PI‐4,5‐P2 and PI‐4,5‐P2‐producing enzymes in cellular invasion by S. aureus. PI‐4,5‐P2 accumulated upon contact of S. aureus with the host cell, and targeting of an active PI‐4,5‐P2 phosphatase to the plasma membrane reduced bacterial invasion. Knockdown of individual phosphatidylinositol‐4‐phosphate 5‐kinases revealed that phosphatidylinositol‐4‐phosphate 5‐kinase γ (PIP5KIγ) plays an important role in bacterial internalization. Specific ablation of the talin and FAK‐binding motif in PIP5KIγ90 reduced bacterial invasion, which could be rescued by reexpression of an active, but not inactive PIP5KIγ90. Furthermore, PIP5KIγ90‐deficient cells showed normal basal PI‐4,5‐P2 levels in the plasma membrane but reduced the accumulation of PI‐4,5‐P2 and talin at sites of S. aureus attachment and overall lower levels of FAK phosphorylation. These results highlight the importance of local synthesis of PI‐4,5‐P2 by a focal adhesion‐associated lipid kinase for integrin‐mediated internalization of S. aureus. Staphylococcus aureus can invade nonprofessional phagocytes via an FnBP‐fibronectin‐mediated linkage to host cell integrins. Shi et al. demonstrate that the integrin‐associated phosphatidylinositol‐kinase PIP5KIγ90 supports bacterial internalization via local production of phosphatidylinositol‐4,5‐bisphosphate (PIP2). Lack of PIP5KIγ90 results in diminished recruitment and activation of PIP2‐binding, integrin‐associated proteins such as talin and FAK leading to reduced host cell invasion by bacterial pathogens.