Herpes simplex viruses (HSV) infect orofacial and genital mucosa, relying on expression of immunomodulatory viral proteins to evade detection and eradication by resident immune populations. Currently the role of Mucosal-associated invariant T (MAIT) cells during HSV infections, and the impact of viral lesions on the availability of Major Histocompatibility Complex, Class-I-related (MR1) ligands, remain unknown. Nevertheless, our in vitro experiments confirm increased retention of mature MR1 on the plasma membrane of HSV infected cells, which is rapidly and profoundly countered by a multi-pronged, virus-driven inhibition of MR1 protein synthesis and ligand-mediated trafficking. Using techniques including flow cytometry, RT-qPCR, immunoblotting, and high throughput quantitative fluorescence microscopy, we identify downregulation of MR1 transcripts, proteasomal degradation of immature MR1 from the endoplasmic reticulum, and accumulation of mature forms in early endosomal compartments, in HSV infected cells. We identify three viral gene products, namely virion host shutoff (vhs), infected cell protein (ICP)22 and unique short (US)3 protein, that contribute in different ways to this immunomodulatory downregulation of MR1. Some of these viral modulatory mechanisms do not impact classical antigen presentation molecules, reflecting a specific biological imperative to minimise surface MR1. This inhibition of MR1 by HSV potentially protects infected cells from early TCR-mediated effector functions such as MAIT cell cytolytic killing of virally infected cells or those during co-infection with microbial pathogens that express metabolites presented via MR1, and the synergistic proinflammatory effects from combined TCR independent and dependent activation.