Lack of control over significant events may induce a state of learned helplessness that is characterized by cognitive, motivational, and affective deficits. Although highly relevant in the pathogenesis of several mental disorders, the extent of the cognitive deficits induced by experiences of uncontrollability and the neural mechanisms underlying such deficits in humans remain poorly understood. Using functional magnetic resonance imaging (fMRI), we tested here whether uncontrollability over aversive events impairs subsequent working memory performance and, if so, which neural processes are involved in such deficits. We assessed working memory and the involved neurocircuitry in the MRI scanner before and after participants underwent a task in which they could either learn to avoid electric shocks or had no instrumental control over shocks. Our results show that subjective, but not objective, uncontrollability over aversive events impaired working memory performance. This impact of subjective uncontrollability was linked to altered prefrontal and parahippocampal activities and connectivity as well as decreased crosstalk between frontoparietal executive and salience networks. Our findings show that the perceived uncontrollability over aversive events, rather than the aversive events themselves or the actual, objective control over them, disrupts subsequent working memory processes, most likely through altered crosstalk between prefrontal, temporal, and parietal areas.