This study challenges the concept that herpes simplex virus type 1 (HSV-1) latency represents a silent infection that is ignored by the host immune system, and suggests antigen-directed retention of memory CD8⁺ T cells. CD8⁺ T cells specific for the immunodominant gB_498-505 HSV-1 epitope are selectively retained in the ophthalmic branch of the latently infected trigeminal ganglion, where they acquire and maintain an activation phenotype and the capacity to produce IFN-γ. Some CD8⁺ T cells showed TCR polarization to junctions with neurons. A gB_498-505 peptide-specific CD8⁺ T cell clone can block HSV-1 reactivation from latency in ex vivo trigeminal ganglion cultures. We conclude that CD8⁺ T cells provide active surveillance of HSV-1 gene expression in latently infected sensory neurons.