Anti-citrullinated protein autoantibody (ACPA)+ rheumatoid arthritis (RA) is associated with specific HLA-DR genotypes, ectopic lymphoid follicles producing ACPA in synovial tissue (ST) and synovial expansion of CD4+ effector-memory, including peripheral helper, T cells. Some clonally expanded ST CD4+ T cells in early RA respond to viral antigens. CD8+granzyme-K+ cytotoxic T lymphocytes (CTL) also infiltrate ST in established RA, while lymph node-resident CD8+ T cells in seropositive at-risk individuals or RA are enriched in CD45RO, CD69 and CXCR5. To address the ST TCR repertoire in ACPA+ HLA-DRB1*04:01+ DMARD-naive early RA, we assessed T cell clonotypes and their location in ST. A large proportion of clonally-expanded T cells in peripheral blood (PB) and ST had signatures of polyfunctional CD4+ or CD8+ CTL expressing TNF, IFNG, GZMK, GZMA and GZMB. A smaller number of CD4+ T cell clonotypes unique to ST had Th2-like (expressing GATA3) and central memory-like transcriptomic profiles, with evidence of IL-6-signaling (expressing CCR7, ICOS, IL6ST). In-silico prediction of CMV epitope recognition by clonally-expanded CD8+ TCR sequences was confirmed with a CMV-specific tetramer. Perivascular clonotypic GZMB+CD8+ T cells were co-located with CD4+ T cells, dendritic cells (DCs) and Thy1+ fibroblasts. In a mouse model of latent mCMV, antigen-induced arthritis (AIA) was more severe, with increases in IFN-γ and TNF production by OVA-specific and mCMV-specific lymph-node T cells, than uninfected OVA-AIA mice. These data suggest that positive feedback from viral-specific T cells may enhance arthritogenic antigen presentation by DCs, and reciprocal enhanced CD4+ T-cell help for CTL and autoantibodies. This hypothesis would advocate strongly for the use of antigen-specific tolerising therapies in regulating bystander responses to promote the control of inflammation in RA.