Memory engram cells, activated by learning, undergo input-specific augmentation in their synaptic connectivity (structure, strength and efficacy) to facilitate memory storage and recall. However, only a subset of these cells is reactivated upon retrieval, indicating potential differences in engram cell synaptic connectivity. In this study, we investigated structural synaptic connectivity differences between reactivated and non-reactivated hippocampal CA1 engram cells under conditions of neutral and aversive contextual memory valence. A combination of eGRASP (enhanced green fluorescent protein (GFP) reconstitution across synaptic partners) and viral TRAP (targeted recombination in activated populations) techniques in mice enabled activity-dependent, input-specific fluorescent tagging of CA3 synapses onto CA1 engram cells during contextual fear conditioning (CFC) or context exposure (CE). After 72 h, mice underwent a retrieval test followed by ex-vivo CA1 engram cell reactivation and spine morphometric analyses. While no differences were observed in the number, or reactivation rate of CA1 engram cells after CFC or CE, experience-dependent differences in spine density and types emerged when comparing reactivated and non-reactivated engram cells within- and between-groups. Specifically, cells encoding neutral contexts exhibit significant decreases in spine density, while cells encoding aversive contexts demonstrate more pronounced shifts towards immature spine types when comparing non-reactivated to reactivated states, respectively. These findings imply that engram cells within a network exhibit diverse paths in structural connectivity depending on the encoded experience and the reactivation status. Future research will focus on elucidating the molecular mechanisms underlying these structural differences.