Background: Depression is one of the most common and debilitating non-motor symptoms of Parkinson's disease (PD). The neurocognitive mechanisms underlying depression in PD are unclear and treatment is often suboptimal. Methods: We investigated the role of striatal dopamine in reversal learning from reward and punishment by combining a controlled medication withdrawal procedure with functional magnetic resonance imaging (fMRI) in 22 non-depressed PD patients and 19 PD patients with past or present PD-related depression. Results: PD patients with a PD-related depression (history) exhibited impaired reward versus punishment reversal learning as well as reduced reward versus punishment-related BOLD signal in the striatum (putamen) compared with non-depressed PD patients. No effects of dopaminergic medication were observed. Conclusions: The present findings demonstrate that impairments in reversal learning from reward versus punishment and associated reward-related striatal signalling depend on the presence of (a history of) depression in PD.