Experiencing stress during adolescence profoundly alters the neural systems that control goal-directed flexible behaviour. These changes are persistent and are thought to drive behavioural inflexibility in adults, a hallmark symptom of several mental illnesses, including addiction, depression, obsessive compulsive disorder and schizophrenia. The ventral hippocampus (vH) is heavily impacted by stress, however, its role in flexible behaviour remains unclear, partially due to its heterogeneity. Thus, the current study investigates how individual vH projection populations contribute to behavioural flexibility and whether stress during adolescence alters their function in adulthood. Using retrograde tracing and patch-clamp electrophysiology in adult mouse brain slices, we find that stress during adolescence alters the vH in a population-specific manner, reducing the activity of vH neurons that project to the prefrontal cortex (PFC). Mimicking this effect in vivo by optogenetically silencing vH-PFC activity impairs flexible behaviour in a probabilistic reversal learning task. Using computational modelling, we reveal that vH-PFC inactivation impairs behaviour by reducing animals’ ability to utilise memories of past outcomes to guide current choices, suggesting that the vH-PFC circuit contributes to behavioural flexibility by integrating past memories to infer current task structure and select optimal actions. Intriguingly, mice that experience stress during adolescence exhibit deficits in flexible behaviour through similar impairments in strategy, suggesting the vH-PFC may be a neural substrate for the negative impacts of adolescent stress on behavioural flexibility. Thus, restoring vH-PFC activity in adults that have experienced stress during adolescence may be a powerful approach to mitigate the behavioural inflexibility they exhibit.