Gamma-aminobutyric acid neurons, born in remote germinative zones in the ventral forebrain (telencephalon), migrate tangentially in two spatially distinct streams to adopt their specific positions in the developing cortex. The cell types and molecular cues that regulate this divided migratory route remains to be elucidated. Here we show that embryonic vascular networks are strategically positioned to fulfil the task of providing support as well as critical guidance cues that regulate the divided migratory routes of gamma-aminobutyric acid neurons in the telencephalon. Interestingly, endothelial cells of the telencephalon are not homogeneous in their gene expression profiles. Endothelial cells of the periventricular vascular network have molecular identities distinct from those of the pial network. Our data suggest that periventricular endothelial cells have intrinsic programs that can significantly mould neuronal development and uncovers new insights into concepts and mechanisms of central nervous system angiogenesis from both developmental and disease perspectives.