We report that oral infection with Yersinia pseudotuberculosis results in the development of two distinct populations of pathogen-specific CD8⁺ tissue-resident memory T cells (T_RM cells) in the lamina propria. CD103⁻ T cells did not require transforming growth factor-β (TGF-β) signaling but were true resident memory cells. Unlike CD103⁺CD8⁺ T cells, which were TGF-β dependent and were scattered in the tissue, CD103⁻CD8⁺ T cells clustered with CD4⁺ T cells and CX3CR1⁺ macrophages and/or dendritic cells around areas of bacterial infection. CXCR3-dependent recruitment of cells to inflamed areas was critical for development of the CD103⁻ population and pathogen clearance. Our studies have identified the 'preferential' development of CD103⁻ T_RM cells in inflammatory microenvironments within the lamina propria and suggest that this subset has a critical role in controlling infection.