Multiple neuronal functions require decentralized processes including activity-dependent localized protein synthesis. However, how local protein synthesis drives the dendritic remodeling is still elusive. Kinesin superfamily proteins (KIFs) are microtubule-based motor proteins that transport various types of cargos to a specific area where they function. This intracellular transport system is essential for neuronal morphogenesis, function, and survival. KIF17 and KIF5A are abundantly expressed in neurons and have been suggested to transport NMDAR and AMPAR in neuronal dendrites, respectively. CaMKII-dependent phosphorylation of KIF17 triggered by NMDAR-mediated activity regulates its capacity for binding/release of NR2B-containing vesicles, and acute increase in intracellular Ca2+ through NMDAR regulates the speed of AMPAR transport. Thus, we hypothesized that KIF17 and KIF5A might be functionally regulated by NMDAR-mediated neuronal activity. Here, we show that KIF17 is rapidly degraded by the proteasome and subsequently synthesized at dendritic shafts in an NMDAR-mediated activity-dependent manner. Accompanied by the degradation of KIF17, its transport is temporarily dampened in dendrites. We also report that activity-dependent local KIF17 and KIF5A synthesis driven by its 3' untranslated region (3'UTR) occur at dendritic shafts, and the newly synthesized KIF17 moves along the dendrites. Furthermore, hippocampus-specific deletion of Kif17 3'UTR led to impairment in extinction of fear memory. These results suggest that the regulation of the transport by KIF17 and KIF5A is driven by the single dendrite-restricted mechanism including local protein synthesis that underlies cognitive flexibility. This model could help further understanding how a single dendrite serves as the computational unit for the memory process.