Neurons are compartmentalized into two molecularly and functionally distinct domains, axons and dendrites. The precise targeting and localization of proteins within these domains is critical for every aspect of neuronal function. α-Amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA)-type glutamate receptors are composed of heteromeric combinations of GluA1 to GluA41 and are the major excitatory neurotransmitter receptors in the central nervous system. The diversity in regulation of AMPA receptor subunit expression suggests that changes in the properties of AMPA receptors serve specific functions in a variety of brain areas. Altering the level of AMPA receptor activity has also been shown to play an important role in dendritic patterning and synapse maturation and formation, and disturbance of AMPA receptor localization has been implicated in many psychiatric and neurological disorders. However, little is known about how extrinsic molecules regulate the dendritic localization of AMPA receptors. Here we show that Semaphorin3A (Sema3A) signaling at the axonal growth cone is propagated toward the cell body by retrograde axonal transport and drives AMPA receptor GluA2 to the distal dendrites, which regulates dendritic development. Sema3A enhances glutamate receptor interacting protein 1-dependent localization of GluA2 in dendrites, which is blocked by knockdown of cytoplasmic dynein heavy chain. PlexinA (PlexA), a receptor component for Sema3A, interacts with GluA2 at the immunoglobulin-like Plexin-transcription-factor domain (PlexA-IPT) in somatodendritic regions. Overexpression of PlexA-IPT suppresses dendritic localization of GluA2 and induces proximal bifurcation phenotype in the apical dendrites of CA1 hippocampal neurons. Thus, we propose a novel control mechanism by which retrograde Sema3A signaling regulates the glutamate receptor localization through trafficking of cis-interacting PlexA with GluA2 along dendrites.