Granulomas are organized immune cell aggregates that form in response to chronic infection or antigen persistence. The bacterial pathogen Yersinia pseudotuberculosis (Yp) blocks innate inflammatory signaling and immune defense, inducing neutrophil-rich pyogranulomas within lymphoid tissues. However, whether pyogranulomas contribute to control of enteropathogenic Yersinia at the intestinal barrier was previously unknown. Through the work in this dissertation, we uncover that Yp triggers pyogranuloma formation within the murine intestinal mucosa. Monocyte-lineage cells were critical for granuloma-mediated control of Yp, as mice lacking circulating monocytes fail to form defined pyogranulomas and succumb to Yp infection. Yersinia lacking YopE and YopH, virulence factors that target actin polymerization to block phagocytosis and reactive oxygen burst, do not induce pyogranulomas, indicating that intestinal pyogranulomas form in response to Yp blockade of the host immune response. Mutation of YopH restores pyogranuloma formation and control of Yp in mice lacking circulating monocytes, demonstrating that monocytes overcome YopH-dependent blockade of innate immune defense. Additionally, we demonstrate that the pro-inflammatory cytokine tumor necrosis factor (TNF) is required for monocyte-mediated control of Yp within intestinal pyogranulomas. We find that TNF signals in an autocrine manner to drive monocyte-intrinsic production of interleukin-1 (IL-1), which signals through IL-1 receptor on non-hematopoietic cells to enable formation of intact pyogranulomas and control of Yersinia infection. We uncover a TNF-IL-1 circuit as a crucial driver of intestinal granuloma formation and function, mechanistically defining the cellular source and target of TNF signaling that restricts intestinal Yersinia infection. Overall, this work reveals an unappreciated site of Yersinia intestinal invasion and defines host and pathogen drivers of intestinal granuloma formation. These findings increase our understanding of granuloma-mediated restriction of pathogens and may have implications for the development of therapeutics that enhance pathogen control within granulomas or suppress granulomatous inflammation in the context of autoimmune and inflammatory disease.