During embryonic and postnatal development of the dentate gyrus (DG), neural stem cells (NSCs) proliferate, migrate and generate mature granule neurons. Unlike other brain regions, NSCs remain in the adult DG, mostly in a state of deep quiescence, with the ability to re-enter cell cycle and generate new neurons throughout life. The transitions back and forward from a proliferative state to a temporal shallow quiescence or primed state ensure the maintenance of stem cell population. However, it is unclear when and how adult NSCs acquire quiescence sub-states during development. Recently, we have determined that transcription factor Sox5 is required for the transition from quiescence to activation in adult NSCs and for the generation of new neurons (Li, Medina-Menéndez et al., 2022). Now, using conditional mouse mutants for Sox5 during embryonic (Sox5Nestin) or early postnatal development (Sox5Sox2-creERT), we describe a critical window around P14 when NSCs build up a primed quiescent state (pqNSCs). During that period, an excess in pqNSCs leads to aberrantly over activated NSCs and an excess in neurogenesis in Sox5 mutant adult DG. These alterations lead in mature adult Sox5Nestin mice to a premature reduction of the NSC pool and a decrease in adult neurogenesis. Finally, we have uncovered the involvement of the TGBβ/BMP signaling pathway in the early establishment of the pqNSCs population and how Sox5 loss alters this signaling pathway. In conclusion, we have determined that Sox5 controls the establishment of reduced population of pqNSCs during early DG development that ensures long lasting adult hippocampal neurogenesis.