Musical training and bilingualism benefit executive functioning and working memory (WM)—however, the brain networks supporting this advantage are not well specified. Here, we used functional magnetic resonance imaging and the n‐back task to assess WM for spatial (sound location) and nonspatial (sound category) auditory information in musician monolingual (musicians), nonmusician bilinguals (bilinguals), and nonmusician monolinguals (controls). Musicians outperformed bilinguals and controls on the nonspatial WM task. Overall, spatial and nonspatial WM were associated with greater activity in dorsal and ventral brain regions, respectively. Increasing WM load yielded similar recruitment of the anterior‐posterior attention network in all three groups. In both tasks and both levels of difficulty, musicians showed lower brain activity than controls in superior prefrontal frontal gyrus and dorsolateral prefrontal cortex (DLPFC) bilaterally, a finding that may reflect improved and more efficient use of neural resources. Bilinguals showed enhanced activity in language‐related areas (i.e., left DLPFC and left supramarginal gyrus) relative to musicians and controls, which could be associated with the need to suppress interference associated with competing semantic activations from multiple languages. These findings indicate that the auditory WM advantage in musicians and bilinguals is mediated by different neural networks specific to each life experience.