Group A Streptococcus (GAS) infection-associated immune disorders have been long known but how T cells are involved in their pathogenesis is largely unexplained. CD1a presents lipid antigens to T cells, but the potential relevance to GAS infection has not been studied. Here, we investigated whether GAS-responsive CD1a-restricted T cells contribute to the pathogenesis of psoriasis, a chronic inflammatory skin disease. Healthy individuals had high frequencies of circulating and cutaneous GAS-responsive CD4+ and CD8+ T cells with rapid effector functions, including the production of interleukin-22 (IL-22). Human skin and blood single-cell CITE-seq analyses of IL-22–producing T cells showed a type 17 signature with proliferative potential, whereas IFN-γ–producing T cells displayed cytotoxic T lymphocyte characteristics. These GAS-responsive T cells were expanded and activated in patients with psoriasis, and can react to self-antigens, such as lysophosphatidylcholine (LPC). Furthermore, GAS infection in humanized CD1a transgenic mice drove an enhanced and prolonged psoriasis-like phenotype. Together, these findings link GAS infection to the CD1a pathway and show that GAS infection promotes the proliferation and activation of CD1a-autoreactive T cells, with relevance to post-streptococcal disease, including the pathogenesis and treatment of psoriasis.