The neocortex, which is hallmark of mammals, controls essential brain functions via a remarkable architecture of its internal microcircuits as well as via an extensive wiring with the rest of the brain. In particular, topographically organized thalamocortical connections convey sensory and motor input from the periphery to distinct areas of the neocortex. During embryonic development, thalamocortical projections establish a blueprint of the neocortical extrinsic connectivity, which can be remodeled postnatally. Understanding how these projections are formed is essential not only to progress in our comprehension of neural wiring and neocortical functioning, but also to unravel the mechanisms underlying the “high-jacking” of major functions by the neocortex during the evolutionary emergence of the mammalian brain. We previously showed that mouse thalamocortical connections are guided internally towards the neocortex by the tangential migration of guidepost “corridor” neurons in an intermediate target. Here, we show that corridor neurons act as a hub to orient the topographic positioning of thalamocortical projections towards distinct cortical areas, by expressing combination of guidance cues that elicit expected and paradoxical responses in thalamic axons. These results reveal a novel function of cell migration in the internal pathfinding and topographic orientation of thalamocortical projections and raise the question of how this process emerged during evolution. Using comparative studies in mammals, reptiles & birds, as well as functional experiments, we found that species-specific differences in the migration of conserved corridor neurons regulate the opening of a mammalian neocortical route for thalamic axons. We further show that the midline repellent Slit2 orients the migration of corridor neurons and thereby switches the position of thalamic axons to a mammalian-specific path. Our study reveals that subtle differences in the migration of conserved intermediate neurons trigger large-scale changes in thalamic connectivity, and opens novel perspectives on the development and evolution of brain wiring.