Infections of the CNS represent a significant predisposing factor for the manifestation of acute and chronic seizures. Epilepsy is associated with hippocampal sclerosis and neuronal degeneration; thus a regenerative approach could constitute a novel therapeutic option, involving the promotion of adult neurogenesis within the subgranular zone of the dentate gyrus (DG). Although experimental seizures induced by chemoconvulsants or electrical stimulation transiently enhance neurogenesis, the implications of encephalitis and virus-induced seizures remain inadequately elucidated. Accordingly, we employed the Theiler’s Murine Encephalomyelitis Virus (TMEV) model to delineate the acute and chronic effects of infection-induced seizures on neurogenesis. Despite an unaltered overall proliferation of cells following infection, distinctive proliferation patterns emerged between TMEV and control (CTR) mice: (1) Neuronal progenitors (DCX+) were virtually absent at 3 days post-infection (dpi) and did not replenish to CTR levels until 90 dpi. They showed early aberrant migration patterns, already observed by 14 dpi. (2) Proliferating neural stem cells significantly decreased close to the injection site of TMEV at 14 dpi compared to CTR. (3) A heightened population of proliferating astrocytes was noted. The observed changes in neurogenesis were seen in all TMEV-infected mice, independent of acute or chronic seizures. In summary, our findings demonstrate that viral infection rapidly depletes neuronal progenitor cells and induces aberrant migration, potentially contributing to hyperexcitability. Moreover, the heightened differentiation towards glial cell fate in infected mice emerges as an additional putative pro-epileptogenic mechanism.