The identification and characterization of esophageal stem cells are critical to our understanding of the biology of the esophageal epithelium in health and disease. However, the proliferative compartment within the mouse esophageal epithelium remains poorly characterized. Here, we report that the basal cells of the mouse esophagus can be separated into three phenotypically and functionally distinct subpopulations based on the expression of α₆ integrin and transferrin receptor (CD71). Cells that express high levels of α₆ integrin and low levels of CD71, termed α₆^briCD71^dim, are a minor subpopulation of small and undifferentiated cells that are enriched for label-retaining cells and thus represent a putative esophageal stem cell population. Conversely, cells expressing high levels of both α₆ integrin and CD71 (α₆^briCD71^bri), the majority of basal esophageal cells, are enriched for actively cycling cells and therefore represent a transit-amplifying population. Kinetic analyses revealed that a third cell population, which is α₆ integrin-dim and CD71-bright (α₆^dim), is destined to leave the basal layer and differentiate.