In the neocortex, higher-order areas are essential to integrate sensory-motor information and have expanded in size during evolution. How higher-order areas are specified, however, remains largely unknown. Here, we show that the migration and distribution of early-born neurons, the Cajal-Retzius cells (CRs), controls the size of higher-order areas in the mouse somatosensory, auditory, and visual cortex. Using live imaging, genetics, and in silico modeling, we show that subtype-specific differences in the onset, speed, and directionality of CR migration determine their differential invasion of the developing cortical surface. CR migration speed is cell autonomously modulated by vesicle-associated membrane protein 3 (VAMP3), a classically non-neuronal mediator of endosomal recycling. Increasing CR migration speed alters their distribution in the developing cerebral cortex and leads to an expansion of postnatal higher-order areas and congruent rewiring of thalamo-cortical input. Our findings thus identify novel roles for neuronal migration and VAMP3-dependent vesicular trafficking in cortical wiring. Display omitted •Subtype-specific migration kinetics determine CRs cortical distributions•Inhibiting VAMP3 increases migration speed, but not directionality, of CR subtypes•VAMP3-dependent vesicular trafficking regulates CR cortical dispersion•Altered CRs distribution changes the size and wiring of higher-order cortical areas Barber et al. find that vesicular trafficking modulates the migration speed and cortical distributions of Cajal-Retzius neurons. They show that CR composition influences the size and wiring of postnatal visual, auditory, and somatosensory systems. These findings implicate VAMP3 in CR migration and in the patterning of higher-order cortical areas.