MR1 presents riboflavin-related microbial metabolites and folate-derivatives to MAIT-cells, but it was unknown whether MR1 could present alternative antigens to other T cell lineages. We identified a novel population of human T cells (which we called MR1T cells), present in genetically different healthy individuals, displaying diverse TCR α and β chains and recognizing MR1-expressing cells in the absence of microbial ligands. Analysis of MR1T cell clones revealed specificity for distinct cell-derived antigens and alternative transcriptional strategies for metabolic programming, cell cycle control and functional polarization following antigen stimulation. Phenotypic and functional characterization of MR1T cell clones showed multiple chemokine receptor expression profiles and secretion of diverse effector molecules, suggesting functional heterogeneity. Accordingly, MR1T cells exhibited distinct T helper-like capacities upon MR1-dependent recognition of target cells expressing physiological levels of surface MR1. These data extend the role of MR1 beyond microbial antigen presentation and indicate MR1T cells are a normal part of the human T cell repertoire.