T cell factor 1 (Tcf-1) expressing CD8 ⁺ T cells exhibit stem-like self-renewing capacity, rendering them key for immune defense against chronic viral infection and cancer. Yet, the signals that promote the formation and maintenance of these stem-like CD8 ⁺ T cells (CD8 ⁺ SL) remain poorly defined. Studying CD8 ⁺ T cell differentiation in mice with chronic viral infection, we identified the alarmin interleukin-33 (IL-33) as pivotal for the expansion and stem-like functioning of CD8 ⁺ SL as well as for virus control. IL-33 receptor (ST2)-deficient CD8 ⁺ T cells exhibited biased end differentiation and premature loss of Tcf-1. ST2-deficient CD8 ⁺ SL responses were restored by blockade of type I interferon signaling, suggesting that IL-33 balances IFN-I effects to control CD8 ⁺ SL formation in chronic infection. IL-33 signals broadly augmented chromatin accessibility in CD8 ⁺ SL and determined these cells' re-expansion potential. Our study identifies the IL-33-ST2 axis as an important CD8 ⁺ SL-promoting pathway in the context of chronic viral infection.