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 (TRM 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? TRM cells in inflammatory microenvironments within the lamina propria and suggest that this subset has a critical role in controlling infection.