Memories are dynamic constructs whose properties change with time and experience. The biological mechanisms underpinning these dynamics remain elusive, particularly concerning how shifts in the composition of memory-encoding neuronal ensembles influence a memory properties’ evolution over time. Here we leveraged a developmental approach to target distinct subpopulations of principal neurons (“birthdated neurons”), and used calcium imaging, optogenetics, chemogenetics, in association with multiple hippocampus-dependent learning tasks to investigate their contribution to memory engrams over time. Our results show that (1) different subpopulations of developmentally-defined neurons in the hippocampus have distinct recruitment dynamics to the engram during memory consolidation, recent, and remote recall, while divergent recruitment of birthdated neurons is not observed in the amygdala and subiculum; (2) birthdated neurons in CA3 segregate into separate subnetworks with distinct physiological properties, co-firing dynamics, and capacity for plasticity, and (3) exhibit divergent activity dynamics upon the processing of a fear memory; (4) the recruitment of CA3, but not CA1, birthdated neurons at specific delays after acquisition is necessary for successful memory retrieval; and (5) the recruitment of a transient memory trace in CA3, but not CA1, supports plasticity of recently-acquired memories. Together, our results indicate that the divergent recruitment of functionally segregated populations in hippocampal CA3, which are rooted in neurogenesis, can support various memory functions over time, and reveal possible mechanisms by which information across multiple temporally adjacent learning episodes can be integrated into cohesive memories.