Cytotoxic T-cells become progressively dysfunctional within tumors due to chronic antigen-dependent initiation of a genome-wide epigenomic and transcriptional program known as T-cell “exhaustion”. Whether and how cellular metabolism has a role in modulating the differentiation and phenotype of exhausted T-cells (Tex) has marginally been explored. To determine how metabolism could influence T-cell exhaustion, we initially characterized the metabolic profile and secretome of Tex. We found phenylpyruvic acid (PP), a catabolite of phenylalanine, amongst the most significantly upregulated metabolites in Tex and culture media. The immune modulatory enzyme interleukin 4 induced 1 (IL4I1), was identified as the main source of PP. IL4I1 is significantly increased in T-cells across various contexts, including in vitro chronic TCR stimulation, LCMV-mediated chronic viral infection and murine tumor models. Recently, IL4I1 was implicated in producing agonists of the aryl hydrocarbon receptor (AHR), a known to regulator of the phenotype and differentiation of various cell types. Transcriptome analysis revealed that Tex exhibit increased AHR activity. Using in vitro and in vivo models, we evaluated the effect of IL4I1 and AHR modulation on the immunophenotype, cytotoxic capacity, proliferation and metabolism of mouse and human Tex. Our results identify IL4I1 and AHR as metabolic biomarkers active in Tex and suggest them as targets than can synergize with current immunotherapies.