Regulatory T cell (Treg) therapy is a promising curative approach for autoimmunity and transplant rejection, in which there is pathological tissue damage. Enabling Tregs to directly promote tissue repair in cell therapy would be attractive for a variety of clinical settings. In mice, Tregs drive tissue repair after infection or injury via production of the growth factor amphiregulin—a process controlled by the alarmins IL-18 or IL-33 and its receptor ST2. We investigated the tissue repair potential of human Tregs via IL-33/ST2 and amphiregulin. We found that human Tregs in blood and multiple tissue types could produce amphiregulin ex vivo, but this feature was neither specific to Tregs nor upregulated in tissues. Amphiregulin-producing human Tregs were enriched for a naive, non-effector phenotype and were progressively lost upon TCR-mediated proliferation and differentiation. In ex vivo blood Tregs, amphiregulin production was not induced by IL-18, and these cells did not express ST2 and hence did not respond to IL-33. Human ST2+ Tregs were also not detected in tonsil, synovial fluid, colon, or lung tissue. Meanwhile, human Tregs engineered to overexpress ST2 recapitulated canonical IL-33 signalling; in these cells, IL-33 innately upregulated amphiregulin expression but did not affect their TCR-dependent suppressive capacity. Collectively, human tissue-reparative Tregs may function innately and more research is required to understand the role of IL-33 in this process. Future work will investigate other pathways beyond IL-33/ST2 in controlling this function and examine the tissue repair capacity of human Treg-derived amphiregulin in vitro.