The study investigates the role of CXCL12+ dermal fibroblasts in neutrophil recruitment and host defense against *Staphylococcus aureus* (S. aureus) infection. Single-cell RNA sequencing (scRNA-Seq) and network analysis of mouse skin during S. aureus infection revealed that CXCL12+ fibroblast subsets, primarily found in the reticular dermis, play a dominant role in communicating with neutrophils. These fibroblasts express IL-17 signaling and adipocyte lineage markers, detect IL-17 and TNFα, and promote neutrophil recruitment through NFKBIZ-dependent release of CXCR2 ligands and CXCL12. In vitro experiments using 3T3-L1 preadipocyte fibroblasts confirmed that IL-17A and TNFα synergistically activate these fibroblasts, leading to the production of neutrophil chemokines and antimicrobials. In vivo studies in mice lacking IL-17RA specifically in fibroblasts showed reduced neutrophil recruitment and increased S. aureus infection. Similar findings were observed in a psoriasis model, where CXCL12+ fibroblast subsets expressed high levels of neutrophil chemokines. These results highlight the critical role of CXCL12+ dermal fibroblasts in cutaneous neutrophil recruitment and host defense, suggesting that these fibroblasts contribute to both infectious and non-infectious forms of skin inflammation.The study investigates the role of CXCL12+ dermal fibroblasts in neutrophil recruitment and host defense against *Staphylococcus aureus* (S. aureus) infection. Single-cell RNA sequencing (scRNA-Seq) and network analysis of mouse skin during S. aureus infection revealed that CXCL12+ fibroblast subsets, primarily found in the reticular dermis, play a dominant role in communicating with neutrophils. These fibroblasts express IL-17 signaling and adipocyte lineage markers, detect IL-17 and TNFα, and promote neutrophil recruitment through NFKBIZ-dependent release of CXCR2 ligands and CXCL12. In vitro experiments using 3T3-L1 preadipocyte fibroblasts confirmed that IL-17A and TNFα synergistically activate these fibroblasts, leading to the production of neutrophil chemokines and antimicrobials. In vivo studies in mice lacking IL-17RA specifically in fibroblasts showed reduced neutrophil recruitment and increased S. aureus infection. Similar findings were observed in a psoriasis model, where CXCL12+ fibroblast subsets expressed high levels of neutrophil chemokines. These results highlight the critical role of CXCL12+ dermal fibroblasts in cutaneous neutrophil recruitment and host defense, suggesting that these fibroblasts contribute to both infectious and non-infectious forms of skin inflammation.