A clinically distinct subset of rheumatoid arthritis (RA) is characterised by production of anti-citrullinated peptide autoantibodies and subsequent chronic autoimmune joint inflammation. Multiple lines of evidence point to T cells as key players in the inflammatory pathogenesis. However, it is currently unclear what type of T cells are involved in the joints in the early stages of disease, and what their specific targets are. With the advent of single cell and T cell receptor sequencing technologies, we studied the blood and synovial tissue of recent-onset untreated RA patients, to investigate T cell transcriptome and T cell receptor. A proinflammatory population of cytotoxic T cells was enriched in joint synovial tissue in all 4 patients studied. Intriguingly, their T cell receptors had been identified previously to be specific for viral antigen recognition, particularly the chronic viral infections, EBV and CMV. These T cells comprised the overwhelming majority of circulating T cell clones, and some of these were shared in synovial tissue, thus reflecting T cell recruitment into the joint. In the absence of viral infection in the joint, these T cells represent “bystander inflammatory T cells”. In addition to these, a small number of expanded CD4+ helper T cell clones were found uniquely in the synovial tissue. We hypothesize that these cells may recognize rheumatoid arthritis-related synovial antigens. Our findings suggest that at disease onset, joint inflammation is propagated by T cells that have expanded to manage chronic viral infections, which infiltrate the joint synovial tissue as bystanders, but have inflammatory capacities to drive collateral joint damage. Similar to previous findings in multiple sclerosis, which is also more common in women, our findings demonstrate the critical importance of immune control of chronic viral infections to the immunopathogenesis of RA and have important implications for the design of future immunotherapies.