Increasing evidence associates apathy with worsening in cognitive performance and greater risk of dementia, in both clinical and healthy older populations. In older adults with neurocognitive disorders, apathy has also been related to specific fronto-subcortical structural abnormalities, thus differentiating apathy and major depressive disorder. Yet, the neural mechanisms associated with apathy in healthy older adults are still unclear. In the present study, we investigated the frontal cortical response during a dual-task walking paradigm in forty-one healthy older adults with and without apathy symptoms, controlling for depressive symptoms. The dual-task walking paradigm included a single cognitive task (2-back), a single motor task (walking), and a dual-task condition (2-back whilst walking). The cortical response was measured by means of functional Near-Infrared Spectroscopy (fNIRS). The results revealed that participants with apathy symptoms showed greater activation of subregions of the prefrontal cortex and of the premotor cortex compared to healthy controls during the single cognitive component of the dual-task paradigm, whilst cognitive performance was equivalent between groups. Moreover, increased cortical response during the cognitive task was associated with higher odds of exhibiting apathy symptoms, independently of depressive symptoms. These findings suggest that apathy may be related to differential brain activation patterns in healthy older individuals and are in line with previous evidence of the distinctiveness between apathy and depression. Future research may explore the long-term effects of apathy on the cortical response in healthy older adults.