The cerebral cortex consists of several hundreds of different types of neurons, organized into specific cortical layers and areas, that display specific profiles of gene expression, morphology, excitability and connectivity. The identification and characterization of factors capable of (re)specifying the identity of cortical neurons has important implications regarding our understanding of neurodevelopmental diseases and in the context of therapies for neurological disorders. Embryonic stem (ES) and other pluripotent stem cells constitute a promising tool for the modelling and treatment of human neural diseases. Here we describe a novel pathway by which pluripotent stem cells, whether of mouse or human origin, recapitulate in vitro the major milestones of cortical development, leading to the sequential generation of a diverse repertoire of neurons that display most salient features of genuine cortical neurons. When grafted into the cerebral cortex of newborn, or lesioned cortex of adult anaesthetised mice, these neurons develop specific patterns of axonal projections corresponding to endogenous cortical projections in vivo. Intrinsic corticogenesis sheds new light on the mechanisms of neuronal specification, and constitutes an innovative tool to model normal and pathological cortical development, including in the human species. In the long run, cortical neurons generated in vitro could be used also in the perspective of brain repair, for several diseases striking cortical neurons.