Cells of the immune system that reside in barrier epithelia provide a first line of defense against pathogens. Langerhans cells (LCs) and CD8⁺ tissue-resident memory T cells (T_RM cells) require active transforming growth factor-β1 (TGF-β) for epidermal residence. Here we found that integrins α_vβ₆ and α_vβ₈ were expressed in non-overlapping patterns by keratinocytes (KCs) and maintained the epidermal residence of LCs and T_RM cells by activating latent TGF-β. Similarly, the residence of dendritic cells and T_RM cells in the small intestine epithelium also required α_vβ₆. Treatment of the skin with ultraviolet irradiation decreased integrin expression on KCs and reduced the availability of active TGF-β, which resulted in LC migration. Our data demonstrated that regulated activation of TGF-β by stromal cells was able to directly control epithelial residence of cells of the immune system through a novel mechanism of intercellular communication.