Breast cancer remains the most widely diagnosed cancer in the world. Greater then 99% of breast cancers arise from a population of progenitor cells within the mammary epithelium. These progenitor cells are highly suspectable to cancer causing mutations in the breast cancer susceptibility genes, BRCA1 and BRCA2. Despite their clear importance, there lacks an understanding of how these progenitors maintain homeostasis in the gland and the molecular mechanisms governing their function. We profiled mammary epithelial cells from embryogenesis through to adulthood and pregnancy by scRNA-seq and uncovered chromatin changes during puberty and in the maintenance of homeostasis in the adult. These data identified that bilineage chromatin patterns within the mammary stems cell are abolished during puberty but reestablished within the mature ducts. In adult mammary cells there is widespread gene priming within the stem cells, with genes poised for upregulation within progenitor and mature cells upon differentiation. In addition, progenitor cells exhibit bilineage chromatin patterns, with active chromatin for the hormone receptor negative (HR–, milk producing lineage) and enhancer priming and bivalent promoters for the HR+ lineage that responds to essential oestrogen and progesterone signalling to drive development. Using HR expression and the most differentially expressed progenitor cell marker, CD14, we redefined the progenitor populations, isolating HR– and HR+ cells, uncovering that in vivo proliferation is contained entirely within this compartment. These studies highlight that the mammary stem cells actively maintain the capacity for differentiation into both epithelial lineages and that within the progenitor pools exists two distinct lineages of cells that are highly proliferative and likely explaining why these cells are the cell-of-origin for the majority of human breast cancers.