Intraepithelial lymphocytes (IELs), including gd and ab T cells are critical for maintaining the intestinal barrier by sensing microbes, nutrients, and cellular stress. Colorectal carcinoma (CRC) is a leading cause of cancer death and there is a critical need to develop biomarkers for disease progression and develop more effective immunotherapies. The factors regulating IEL development and function in the colon are largely unknown, however they have recently been shown to limit CRC progression. We discover distinct IEL transcriptional programs, developmental requirements and effector phenotypes across individual compartments of the mouse and human gastrointestinal tract. Colon IELs specifically expressed the transcriptional regulator TCF-1. Deletion of TCF-1 released a unique IEL effector profile and eliminated tumours in the colon. In human colorectal carcinoma, we show that TCF-1 expression decreases in IELs compared to healthy colon, this strongly correlated with an enhanced IEL effector phenotype and improved patient survival. Our work identifies TCF-1 as a colon specific IEL transcriptional regulator and will inform strategies to develop novel immunotherapies to treat CRC.