In birds, patterns of development of the adrenocortical response to stressors vary among individuals, types of stressors, and species. Since there are benefits and costs of exposure to elevated glucocorticoids, this variation is presumably a product of selection such that animals modulate glucocorticoid secretion in contexts where doing so increases their fitness. In this study, we evaluated hypothalamic-pituitary-adrenal (HPA) activity in first-hatched free-living seabird nestlings (black-legged kittiwakes,Rissa tridactlya) at a critical early age when food availability may drive the establishment of important parent-offspring and intra-brood dynamics. We experimentally supplemented parents with food (fed) and measured chick baseline corticosterone secretion at 5 days post-hatch (of the ~45 day nestling period) and capacity to rapidly increase corticosterone in response to an acute challenge (handling and a 15 min restraint in a bag). We also used topical administration of corticosterone to evaluate the ability of chicks to downregulate physiologically relevant corticosterone levels on a short (minutes) time scale. We found that 5 day old chicks are capable of releasing corticosterone in proportion to the magnitude of the challenge, showing differences in baseline between parental feeding treatments (supplementally-fed vs control), moderate increases in response to handling, and a larger response to restraint (comparable to restraint-induced levels found in adults) that also differed between chicks from fed and control nests. The topical application of exogenous corticosterone resulted in an increase of circulating levels similar to the restraint-induced levels. The corticosterone application also induced the downregulation of HPA responsiveness to the acute challenge of handling. Parental supplemental feeding did not affect absorbance/clearance or negative feedback. Thus, while endogenous secretion of corticosterone in 5 day old chicks is sensitive to environmental context, other aspects of the HPA function, such as rapid negative feedback and/or the ability to clear acute elevations in corticosterone, are not. We conclude that 5 day old kittiwake chicks are capable of robust adrenocortical responses to novel challenges, and are sensitive to parental food availability, which may be transduced behaviorally, nutritionally, or via maternal effects. Questions remain about the function of such rapid, large acute stress-induced increases in corticosterone in very young chicks.