Breast cancer is a heterogeneous disease that is thought to be derived from normal mammary epithelial cells, thus it’s important to understand the organization of the mammary epithelial cell hierarchy and the cell cycle kinetics to understand how these cells relate to the human breast tumours. We have observed that the luminal cell compartment of the mammary gland is more heterogeneous than previously thought and can be resolved into non-clonogenic luminal cells (NCL), relatively differentiated luminal progenitors and relatively undifferentiated luminal progenitors for both mouse and human, and these luminal progenitor populations are highly plastic and can generate progeny representing all mammary cell types. Gene expression profiling demonstrates that the terminally differentiated luminal cell and relatively undifferentiated luminal progenitor subpopulations have signatures that resemble those obtained from luminal A/B and basal-like breast tumours respectively. We have observed that cell division within the mammary epithelium over the long-term is stochastic, but once a cell is recruited into the cell cycle in the estrus cycle, then cell division is repeated. Unexpectedly, most cell division in the adult virgin gland is restricted to a subpopulation of terminally differentiated luminal cells NCL cells that, paradoxically, have traditionally been perceived as being terminally differentiated. Our data also demonstrate that the NCL and the undifferentiated luminal progenitor population have cell division kinetics that are compatible with these populations being largely maintained by their own restricted committed progenitors and not hierarchically organized. We also observe that transplantable stem cells have a cycling status that is linked to the estrus cycle, with these cells undergoing maximal cell division when progesterone levels are high.