There is strong evidence for dissociable “what” and “where” pathways in the auditory system, but considerable debate remains regarding the functional role of these pathways. The sensory-motor account of spatial processing posits that the dorsal brain regions (e.g., inferior parietal lobule, IPL) mediate sensory-motor integration required during “where” responding. An alternative account suggests that the IPL plays an important role in monitoring sound location. To test these two models, we used a mixed-block and event-related functional magnetic resonance imaging (fMRI) design in which participants responded to occasional repetitions in either sound location (“where” task) or semantic category (“what” task). The fMRI data were analyzed with the general linear model using separate regressors for representing sustained and transient activity in both listening conditions. This analysis revealed more sustained activity in right dorsal brain regions, including the IPL and superior frontal sulcus, during the location than during the category task, after accounting for transient activity related to target detection and the motor response. Conversely, we found greater sustained activity in the left superior temporal gyrus and left inferior frontal gyrus during the category task compared to the location task. Transient target-related activity in both tasks was associated with enhanced signal in the left pre- and postcentral gyrus, prefrontal cortex and bilateral IPL. These results suggest dual roles for the right IPL in auditory working memory—one involved in monitoring and updating sound location independent of motor responding, and another that underlies the integration of sensory and motor functions.