Our study investigates mechanisms of epileptogenesis caused by the p.A263V mutation in the SCN2A gene using a Scn2a p.A263V mouse model. The SCN2A gene is known for its role in neurodevelopmental disorders with epileptic presentations. Our objective is to understand the molecular foundations of neonatal neuronal hyperexcitability and its evolution into adult network disruptions, employing scRNA-seq. Neonatal homozygous (hom) mice showed seizures starting around P3, with heterozygous (het) mice also exhibiting early seizures. Despite recovery in het mice, persistent network alterations were observed in both adult hom and het mutants.Advanced computational analyses, including Cacoa for comparison of epileptic vs control hippocampus, CellChat for cell-cell communication, and Lamian for pseudotime analysis, were applied to dissect the transcriptomic landscape across critical developmental stages (P4, P7, P14, P28). These tools helped unravel compositional and expressional changes, as well as the intricate cellular interactions and developmental trajectories underpinning epileptogenesis.Our findings highlighted initial minor transcriptomic shifts in mutant mice at P4 that intensified by P7 into marked neurodevelopmental pathway disruptions. By P14, potential compensatory adaptations emerged in het mice, contrasting the continuous severe alterations observed in hom mice. Progressing to P28, het mice exhibited targeted transcriptomic adjustments, suggesting a subtle cessation of epileptic activity. This trajectory from transient neonatal hyperexcitability to persistent network modifications provides a comprehensive view into the complex interplay of early molecular triggers and long-term neural alterations, offering valuable insights into SCN2A mutation-induced epileptogenesis and informing potential therapeutic interventions.