Reproducibility in morphogenesis relies in part on the precise decoding of positional information by gene regulatory networks and on tissue-scale mechanical coupling to organise cells in space. We characterised the cell biology of an EMT-like process that coordinates the transition of epithelial cells to neural stem cells (NSC) in the Drosophila optic lobe and identified tissue level coordination of epithelium remodelling. We find that emerging NSCs progress through a transitory epithelial-like NSC state, upregulating NSC fate genes while retaining epithelial features such as adherens junctions. These cells, termed epi-NSCs, apically constrict one cell at a time and remain epithelial until they divide asymmetrically to produce the first-born neurons. Apical constriction is associated with contractile myosin pulses and requires the E3 ubiquitin ligase Neuralized and RhoGEF3, both of which are up-regulated in emerging NSCs. Neuralized down-regulates the apical protein Crumbs via its interaction with Stardust. This creates an anisotropy of Crumbs accumulation which is associated with the formation of supracellular junctional myosin cables. Disrupting the regulation of Crumbs by Neuralized led to defects in junctional myosin accumulation and imprecision in the integration of emerging NSCs into the front of epi-NSCs. Neuralized therefore mechanically couples NSC fate acquisition with cell-cell rearrangement to promote precision in morphogenesis and smooth progression of the differentiation front.