Associative layers of the neocortex have greatly expanded during evolution in primates and gyrencephalic species, thus providing them enhanced cortical computational power. In this study, we aimed to identify specific miRs which are evolutionary-relevant for the expansion of associative cortical layers. MiR-137 overexpression strongly expanded the pool of basal intermediate progenitors (bIP) and dramatically shifted the temporal dynamics of neurogenesis towards the production of layer 2/3 associative neurons. More specifically, at early time points (E15.5) miR-137 stimulated the production of neurons by enhancing the neuronal commitment of apical radial glia (aRG). These changes in progenitor dynamics had long term consequences on the postnatal identity of superficial cortical neurons. Analysis of electroporated neurons in the postnatal primary somatosensory cortex revealed that miR-137 promoted the generation of callosal-projecting layer 2/3 neurons and shifted the molecular, morphological and connectivity profile of layer 4 thalamic recipient neurons into layer 2/3-like neurons with transcallosal projections.