FOXG1 is a transcription factor essential for brain development. Mutations in FOXG1 perturb forebrain development and are commonly associated with neurodevelopmental conditions such as autism and epilepsy. These conditions often also co-occur and preliminary studies have suggested a convergent aetiology. Thus studying the biological functions of FOXG1 and providing mechanistic insight into its functions can better reveal the molecular and cellular aetiology of these conditions. This will help us accelerate biomarker discovery and therapeutic strategies for epilepsy in individuals with or without autism. The earliest expression of FOXG1 is in neural stem cells where it is hypothesised to regulate the balance between proliferation and differentiation through its transcriptional effects on neuronal lineage genes. To test this, we differentiated induced pluripotent stem cells (iPSC) into neural precursor cells using 2D cortical rosettes and 3D cerebral organoid models. This revealed that FOXG1 has important biological functions at the earliest stages of neurodevelopment, earlier than previously reported. Specifically, we show that FOXG1 is essential for development of cortical rosette structures (an in vitro 2D neural tube correlate), and loss of FOXG1 disrupted cortical rosette formation and dysregulated key neural lineage genes. Furthermore, initial data suggests these findings are replicated in 3D brain organoids, which are better able to recapitulate prenatal brain development. Here, we found significant alteration in gene expression and regulatory events at a single cell level. This raises the possibility that FOXG1-mediated disruption of brain development processes originate very early on and are guided by gene dysregulations.