Thymic regulatory T cells (tT_regs) are potent inhibitors of autoreactive immune responses, and loss of tT_reg function results in fatal autoimmune disease. Defects in tT_reg number or function are also implicated in multiple autoimmune diseases, leading to growing interest in use of T_reg as cell therapies to establish immune tolerance. Because tT_regs are present at low numbers in circulating blood and may be challenging to purify and expand and also inherently defective in some subjects, we designed an alternative strategy to create autologous T_reg-like cells from bulk CD4⁺ T cells. We used homology-directed repair (HDR)–based gene editing to enforce expression of FOXP3, the master transcription factor for tT_reg. Targeted insertion of a robust enhancer/promoter proximal to the first coding exon bypassed epigenetic silencing, permitting stable and robust expression of endogenous FOXP3. HDR-edited T cells, edT_regs, manifested a transcriptional program leading to sustained expression of canonical markers and suppressive activity of tT_reg. Both human and murine edT_regs mediated immunosuppression in vivo in models of inflammatory disease. Further, this engineering strategy permitted generation of antigen-specific edT_reg with robust in vitro and in vivo functional activity. Last, edT_reg could be enriched and expanded at scale using clinically relevant methods. Together, these findings suggest that edT_reg production may permit broad future clinical application.