During chronic viral infection, virus-specific CD8⁺ T cells become exhausted, exhibit poor effector function and lose memory potential^,,,. However, exhausted CD8⁺ T cells can still contain viral replication in chronic infections^,,,,, although the mechanism of this containment is largely unknown. Here we show that a subset of exhausted CD8⁺ T cells expressing the chemokine receptor CXCR5 has a critical role in the control of viral replication in mice that were chronically infected with lymphocytic choriomeningitis virus (LCMV). These CXCR5⁺ CD8⁺ T cells were able to migrate into B-cell follicles, expressed lower levels of inhibitory receptors and exhibited more potent cytotoxicity than the CXCR5⁻ subset. Furthermore, we identified the Id2–E2A signalling axis as an important regulator of the generation of this subset. In patients with HIV, we also identified a virus-specific CXCR5⁺ CD8⁺ T-cell subset, and its number was inversely correlated with viral load. The CXCR5⁺ subset showed greater therapeutic potential than the CXCR5⁻ subset when adoptively transferred to chronically infected mice, and exhibited synergistic reduction of viral load when combined with anti-PD-L1 treatment. This study defines a unique subset of exhausted CD8⁺ T cells that has a pivotal role in the control of viral replication during chronic viral infection.