Early-life stress can have lifelong consequences, enhancing stress susceptibility and resulting in behavioural and cognitive deficits. While the effects of early-life stress (ELS) on neuronal function have been well-described, we still know very little about the contribution of non-neuronal brain cells to the cellular and behavioural adaptations following ELS. Here, using a rodent model of ELS, we report that astrocytes play a key role in mediating the impact of stress on amygdala-dependent behaviour and synaptic plasticity during adolescence. We report that ELS induces generalisation of fear, associated with increased levels of circulating corticosterone and activation of glucocorticoid receptors in astrocytes. In addition, we identify astrocyte glucocorticoid receptors as targets, mediating ELS-induced cognitive and synaptic impairments. This work establishes astrocytes as key elements in amygdala-dependent memory, and as central mediators of the effects of stress on cognitive function via stress hormone signalling pathways.