Response to immune checkpoint inhibitors in epithelial tumours is often limited to a minority of patients. Recent studies have implicated the tumour microenvironment in resistance to immunotherapies. Cancer-associated fibroblasts (CAFs) are a predominant non-malignant cell population in solid tumours, with a wide range of pro-tumourigenic properties. Of note, CAFs can restrict CD8 T cell infiltration into the tumour epithelium, promote Treg recruitment and differentiation, and delete antigen-specific T cells. Here, we identify a novel targetable mechanism of T cell restriction mediated by CAFs and conserved across four major tumour types: colorectal, breast, pancreatic and prostate carcinomas. CAFs restricted the proliferation of resting and pre-stimulated T cells in a dose-dependent fashion, through provision of soluble factors and independent of Tregs. Inhibition of cyclooxygenase-2 (COX-2) using available drugs (diclofenac, indomethacin, celecoxib) significantly relieved T cell suppression. COX-2 is highly expressed by CAFs, and COX-2+ CAFs co-localised with infiltrating T cells in vivo. COX2-inhibition significantly increased the effector T cell response to anti-PD1 therapy, including production of IL-2 and TNF. Viable colorectal tumour slice assays were used to monitor patient T cell responses within the complex tumour microenvironment, and showed that combination COX-2 inhibition and anti-PD-1 therapy significantly increased T cell proliferation, supporting in vitro results. These data describe a novel CAF-driven immune checkpoint. Targeting CAF-T cell interactions is likely required to unlock the full potential of current and emerging tumour immunotherapies.