The cell division kinetics of mammary stem and progenitor cells is not known. To investigate this, we used quantitative stem and progenitor cell assays in combination with incorporation of synthetic nucleosides to determine the cell division kinetics of the different mammary epithelial cell populations during postnatal mouse mammary development. Our results demonstrate that initial entry into the cell cycle 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 non-clonogenic luminal (NCL) cells that, paradoxically, have traditionally been perceived as being terminally differentiated. Our data also demonstrate that basal, the undifferentiated luminal progenitor and NCL subpopulations have cell division kinetics and telomere lengths that are not compatible with these populations being hierarchically organized, but instead indicate that these populations largely maintained by their own lineage-restricted committed progenitors. 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.