Despite growing evidence that prolonged episodes of effortful listening can lead to mental fatigue, little work has been done to examine the patterns of brain activation associated with listening over time. In order to gain a better understanding of the nature of listening-related mental fatigue, this study characterized the effects of sustained auditory processing on brain activation in 19 adults with normal hearing. A 50-min, auditory choice paradigm served as the fatiguing task. Mental fatigue was quantified using subjective (self-report) and behavioral (response time and accuracy) measures, as well as event-related potential (ERP) measures indexing motivation (error-related negativity; ERN) and general arousal (N1). Additional electrical neuroimaging analyses were carried out on ERP datasets. Subjective and behavioral results confirmed that participants became fatigued during the auditory task (data from the first 25 min compared with the second 25 min). ERPs revealed changes in neural activity consistent with decreased arousal (reduced N1 amplitude). Topographical analyses indicated decreased brain activation, without a change in underlying neural network configuration. Regions of decreased brain activation, as estimated via electrical neuroimaging, suggested a decrease in attention to task stimulus-response characteristics (reduced activation in regions associated with the dorsal attention network). The decrease in mean N1 amplitude revealed a significant, positive correlation with subjective report of reduced motivation. These findings support existing cognitive and neurophysiological models that suggest mental fatigue builds over time on task, and affects motivation to influence task performance. Furthermore, this study shows sustained auditory processing can elicit mental fatigue, and that dorsal parietal activity might provide a useful method of measuring its effects.