Rheumatoid Arthritis (RA) is primarily considered to be an MHC class II-associated autoimmune disease where effector CD4+ T cell play a role in disease pathogenesis. Infiltrating T cells with expanded T cell receptor (TCR)-β clonotypes, some of which are viral-antigen-reactive, have been identified in synovial tissue (ST) of RA patients. Recently, single cell sequencing technologies have also identified large numbers of CD8+ cytotoxic T lymphocytes (CTL) expressing granzyme B and/or granzyme K infiltrating ST in active, established RA. We used multi-omic tools, including single cell RNA and TCR sequencing and Imaging Mass cytometry, to assess the differential ST cellular landscape and address the contribution of virus-specific CD8+ T cells to the development of inflammatory arthritis. We studied paired peripheral blood and ST of ten drug-naïve patients with recent-onset untreated seropositive RA. ST had either predominant diffuse-myeloid (DM, n=4) or lymphoid (L, n=6) histological pathology. We found CD4-like T, B and myeloid cell transcriptomic features of DM and L ST were distinct. While CD4-like regulatory and CD8+ effector-memory T-cell (TEM), including granzyme B/K clonotypes generally infiltrated ST, cytotoxic CD4-like peripheral helper TCR clonotypes and flare-associated monocytes were enriched in L ST. Remission-associated macrophages were enriched in DM ST. A proportion of CD8+ TCRs in ST mapped to viral epitopes at the HLA-class I-restricted TCR-β level. To evaluate the impact of viral infection or viral-induced CTLs, we modelled antigen-induced arthritis (AIA) in mice with latent murine cytomegalovirus or mice recovered from acute lympho-choriomeningitis virus. AIA was more severe after cleared acute or latent infection, due to viral-induced antigen-specific CD8+ T-cell cross-activation of arthritogenic CD4+ T cells. Thus, putative viral-specific CD8+ TEM have the potential to cross-activate antigen-specific CD4+ T-cell function to perpetuate ST inflammation in RA.