Currently, not much is known about neuronal positioning and the roles of primary cilia in postnatal neurodevelopment. We show that primary cilia of principal neurons undergo marked changes in positioning and orientation, concurrent with postnatal neuron positioning in the mouse cerebral cortex. Primary cilia of early- and late-born principal neurons in compact layers display opposite orientations, while neuronal primary cilia in loose laminae are predominantly oriented toward the pia. In contrast, astrocytes and interneurons, and neurons in nucleated brain regions do not display specific cilia directionality. We further discovered that the cell bodies of principal neurons in inside-out laminated regions spanning from the hippocampal CA1 region to neocortex undergo a slow 'reverse movement' for postnatal positioning and lamina refinement. Furthermore, selective disruption of cilia function in the forebrain leads to altered lamination and gyrification in the retrosplenial cortex that is formed by reverse movement. Collectively, this study identifies reverse movement as a fundamental process for principal cell positioning that refines lamination in the cerebral cortex and casts light on the evolutionary transition from three-layered allocortices to six-layered neocortices.