In the olfactory bulb (OB), odorant receptor-specific input converges into glomeruli. Subsequently, the coding of odor information is fine-tuned by local synaptic circuits within the glomeruli and the deeper external plexiform layer (EPL) in the OB. Deciphering the organization of inhibitory granule cells (GCs) in the EPL relative to the secondary dendrites of projection neurons is pivotal for understanding odor processing. We conducted a detailed investigation of GCs, focusing on the timing of neurogenesis, laminar distribution, and synaptogenesis between GCs and projection neurons. In summary, GCs develop following a developmental continuum with an outside-in maturation pattern from embryogenesis to adulthood. GCs born 1 week after birth display a unique sublayer-specific distribution pattern, marking a transition between embryonic or neonatal and adult stages. Integration into reciprocal synaptic circuits occurred 10 days post-neurogenesis. We conclude that the timing of neurogenesis dictates the anatomical configuration of GCs within the OB, which, in turn, regulates preferential synaptic integration with either mitral cell or tufted cell secondary dendrites.