Astrocytes are necessary for neuronal functionality in the adult brain; but may also support embryonic development of its cytoarchitecture. They are generated after neurons from embryonic radial glial cells, following the gliogenic switch. Regulation of the switch, operated by several transcription factors, is fundamental for allowing coordinated interactions between neurons and glia. We deleted one such factor, Sox9, early during mouse brain development and observed perturbed astrogenesis and a significantly compromised dentate gyrus (DG). We dissected the origin of the defect, targeting Sox9 deletion to either the DG neuronal progenitor domain or the adjacent cortical hem (CH), and identified previously uncharacterized ALDH1L1+ astrocytic progenitors in the CH, which form a fimbrial-specific glial scaffold necessary for neuronal progenitor migration towards the developing DG. Our results highlight the crucial role of SOX9 for astroglial potential and illustrate how formation of a local network, amidst cells originating from adjacent domains, underlays brain morphogenesis.