Using mouse spermatogenesis as a model, we present evidence that stem cell density regulation relies on a feedback mechanism, reminiscent of “quorum sensing” in bacterial populations, in which cells transition reversibly between states biased for renewal and primed for differentiation. Using a modelling-based approach, we show that this mechanism provides predictive insights into stem cell dynamics during steady-state, as well as under perturbed and transplantation conditions. We discuss the potential implications of these findings for the regulation of stem cell density in other epithelial contexts.