Tissue-resident memory T (T_RM) cells, functionally distinct from circulating memory T cells, have a critical role in protective immunity in tissues, are more efficacious when elicited after vaccination and yield more effective antitumor immunity, yet the signals that direct development of T_RM cells are incompletely understood. Here we show that type 1 regulatory T (T_reg) cells, which express the transcription factor T-bet, promote the generation of CD8⁺ T_RM cells. The absence of T-bet-expressing type 1 T_reg cells reduces the presence of T_RM cells in multiple tissues and increases pathogen burden upon infectious challenge. Using infection models, we show that type 1 T_reg cells are specifically recruited to local inflammatory sites via the chemokine receptor CXCR3. Close proximity with effector CD8⁺ T cells and T_reg cell expression of integrin-β8 endows the bioavailability of transforming growth factor-β in the microenvironment, thereby promoting the generation of CD8⁺ T_RM cells.