Exposure to early life stress (ELS) can alter neurodevelopment and is implicated in disease risk in later life, including psychiatric and behavioural disorders. The developing brain is plastic, thus ELS may affect the development trajectory of the brain by altering processes such as neurogenesis. ELS is known to impair adult hippocampal neurogenesis, however, the brain regions, cell types and underlying molecular mechanisms altered by ELS during development are unclear. Using an optogenetic zebrafish model to elevate stress hormone levels, we analysed the effects of ELS on neurogenesis during development in the whole brain. We identify that the hypothalamus is a highly stress-sensitive brain region, where ELS causes precocious development followed by failed maturation and early decline accompanied by impaired feeding, growth, and longevity. In ELS-exposed animals, hypothalamic proliferation is initially increased, the hypothalamus is larger, and one of its associated behavioural functions, feeding, develops early. However, precocious development is followed by a rapid decline. In ELS-exposed fish, excess hypothalamic progenitor cells fail to differentiate, and proliferative radial glia are lost from the hypothalamus. Our data highlight the developmental dynamics of hypothalamic neurogenesis following ELS and indicate that the hypothalamus is a stress-sensitive brain region. Alteration of hypothalamic neurogenesis is a potential mechanism through which ELS exerts its effects on behaviour and its associated pathologies. Further understanding of how stress alters development trajectories at the molecular and cellular level is important to reduce the burden of mental and physical ill health across the life-course.