Tau, a microtubule-associated protein pivotal for neuronal integrity, is actively involved in retinal development, regulating growth, differentiation, and maturation processes. Mutations in tau can lead to misfolded protein and fibrils formation, disrupting cellular processes and damaging retinal tissue. Previous studies have identified pathological hallmarks of tauopathies, such as Frontotemporal Dementia (FTD), in the retina of patients even in the early stage of pathology. However, the precise molecular mechanisms and the direct sequence of events underlying this process remain poorly understood. This study investigates the role of tau during neurogenesis using a human induced pluripotent stem cells (iPSCs) carrying an intronic IVS10+16 tau mutation associated with FTD and its isogenic control. Employing 2D and 3D retinal models, we examine the spatiotemporal development of retinal progenitor cells and post-mitotic neurons performing gene expression and immunofluorescence analysis. Our findings reveal delayed neurogenesis, altered tau isoform expression, and impaired synaptic maturation and organization of pre and postsynaptic components in mutant cultures. Functional analysis of Ca2+ oscillations in 2D cultures indicates reduced frequency of tau mutant retinal neurons. In addition, early development of retinal organoids confirms disrupted neuronal maturation in mutant cultures and an increased expression of 4R tau isoforms, leading to an altered 4R/3R isoform ratio in mutant cultures. These results highlight tau critical role in retinal development and suggest implications for neurodegeneration. Leveraging in vitro models, we provide insights into tau pathology's consequences on retinal cells, paving the way for future interventions to safeguard retinal health and counteract neurodegenerative processes.