Background Healthy aging has been associated with stable emotional well-being and attenuated brain responses to negative stimuli. At the same time, depressive symptoms are common in older adults. The neural mechanisms behind this paradox remain to be clarified. We hypothesized that acute stress could alter emotion processing in healthy aging brain and constitute a pathway to vulnerability. Methods Using a randomized, controlled crossover design, we explored the influence of acute stress on brain responses to happy and fearful facial expressions in 25 older adults (60–75 years of age) and 25 young (18–30 years of age) control subjects. Groups were matched on trait anxiety and education. Subjects underwent two separate functional magnetic resonance imaging sessions involving acute stress or a control procedure. Results Affective and physiological responses to the stressor were similar between the two age groups. On a whole-brain level, we revealed a significant age by stress interaction in the fusiform gyrus, indicating a selective enhancement of neural activity with stress in elderly subjects only. When specifically aiming analysis at the amygdala, we found the same stress-related increase in activity in elderly subjects only. Modulation of amygdala reactivity due to stress correlated with trait conscientiousness in elderly subjects exclusively. Conclusions Compared with younger adults, healthy older adults showed increased responsivity of brain regions involved in face and emotion processing while stressed. These findings suggest that increased reactivity of this neural circuitry after acute stress may constitute one mechanism by which emotional well-being during healthy aging could rapidly change into heightened vulnerability for affective disorders.