Cancer-associated fibroblasts (CAFs) are a major population of tumour-resident cells that sequester T cells and strongly correlate with immunotherapy resistance and poor patient outcomes. Here we report that human CAFs from colorectal, breast and pancreatic cancers significantly suppressed the proliferation and function of pre-activated T cells in a constitutive, dose-dependent mechanism. Investigation revealed the inflammation-driven synthase cyclooxygenase 2 (COX2) to be a conserved mediator of CAF-driven T cell suppression in all tumour types tested. COX2 is a key synthase required for the production of eicosanoids and prostanoid, including prostaglandin E2 (PGE2). Within human colorectal tumours, COX2+ CAFs colocalised with T cells. The suppressive interaction was MHC independent. An investigation of T cell intrinsic outcomes revealed a reduction in T cells entering the S phase of the cell cycle. Suppression occurred at physiologically relevant ratios of CAFs to T cells. A range of clinically approved COX inhibitors, including those highly specific for COX2, were effective at blocking the interaction. Together, this work shows that CAFs are able to suppress T cells via the production of prostaglandins; that the mechanism is druggable and highly conserved between tumours, tissues and patients. This work defines a conserved microenvironment-driven T cell suppressive checkpoint.