CD8 T cell expansions and functions rely on glycolysis, but the mechanisms underlying CD8 T cell glycolytic metabolism remain elusive. Here, we show that acylglycerol kinase (AGK) is required for the establishment and maintenance of CD8 T cell metabolic and functional fitness. AGK deficiency dampens CD8 T cell antitumor functions in vivo and perturbs CD8 T cell proliferation in vitro. Activation of phosphatidylinositol-3-OH kinase (PI3K)-mammalian target of rapamycin (mTOR) signaling, which mediates elevated CD8 T cell glycolysis, is tightly dependent on AGK kinase activity. Mechanistically, T cell antigen receptor (TCR)- and CD28-stimulated recruitment of PTEN to the plasma membrane facilitates AGK-PTEN interaction and AGK-triggered PTEN phosphorylation, thereby restricting PTEN phosphatase activity in CD8 T cells. Collectively, these results demonstrate that AGK maintains CD8 T cell metabolic and functional state by restraining PTEN activity and highlight a critical role for AGK in CD8 T cell metabolic programming and effector function.