κ-opioid receptor (KOR) is detected pre- and postsynaptically, but the subcellular localization, translation, and regulation ofkormRNA in presynaptic compartments of sensory neurons remain elusive.In situhybridization detected axonal distribution ofkormRNA in primary neurons of dorsal root ganglia (DRG). The MS2-fused GFP trackedkormRNA transport from DRG neuronal soma to axons, requiring its 5′ and 3′ UTRs. In Campenot chambers, axonal translation ofkormRNA was demonstrated for DRG neurons, which depended on its 5′ UTR and was stimulated by KCl depolarization. KCl depolarization of DRG neurons rendered redistribution ofkormRNA from the postpolysomal fraction to the translationally active polysomal fraction. This study provided evidence for mRNA transport and regulation of presynaptic protein synthesis of nonstructural proteins like KOR in primary sensory neurons and demonstrated a mechanism of KCl depolarization-stimulated axonal mRNA redistribution for localized translational regulation.