The corpus callosum is the central conduit of communication for pyramidal neurons of the neocortex. Corpus callosum agenesis is a hallmark of the human disorder FOXG1 syndrome that is caused by mutations in one FOXG1 allele and results in severe intellectual disability. However, roles of FOXG1 in corpus callosum formation remain unknown. We found that Foxg1 in pyramidal neurons plays essential roles in establishing the identity and axon trajectory of callosal projection neurons (CPNs) and generating proper laminar organization in the cortex. Our ChIPseq study revealed that these neuron-specific actions of Foxg1 are achieved by forming a transcription complex with Rp58. This Foxg1-Rp58 complex directly binds and represses several pro-neural and axon guidance genes, including Robo-Slit, orchestrating the acquisition of CPN-defining traits. Furthermore, deletion of one Foxg1 allele specifically in cortical neurons was sufficient to cause reduction and misprojection of CPNs. This study reveals a novel gene regulatory pathway that specifies a constellation of neuronal characteristics during cerebral cortex development and sheds light on the etiology of FOXG1 syndrome.