In this study, we demonstrate that canonical Wnt signaling is active in dendritic bundle-forming layer 2 pyramidal neurons of the rat retrosplenial cortex during dendritic branching and spine formation. Transient downregulation of canonical Wnt transcriptional activity during the early postnatal period results in a significant irreversible decrease in dendritic complexity that leads to long-lasting deficits in spatial navigation and spatial memory in the adult. During the late phase of dendritogenesis, transient downregulation of canonical Wnt signaling results in decreased spine density and impaired maturation, as well as reduction in both excitatory and inhibitory synapse densities. Finally, we identified neurotrophin-3 (NT3) as a canonical Wnt target gene in regulating dendritogenesis and rescued both dendritic arbor and spine defects by NT3 overexpression. Together, these results reveal a novel role for canonical Wnt transcriptional activity in dendritic development of layer 2 pyramidal neurons in vivo.