Working memory (WM) needs to protect current content from interference and simultaneously be amenable to rapid updating with newly relevant information. An influential model suggests these opposing requirements are met via a BG–thalamus gating mechanism that allows for selective updating of PFC WM representations. A large neuroimaging literature supports the general involvement of PFC, BG, and thalamus, as well as posterior parietal cortex, in WM. However, the specific functional contributions of these regions to key subprocesses of WM updating, namely, gate opening, content substitution, and gate closing, are still unknown, as common WM tasks conflate these processes. We therefore combined fMRI with the reference-back task, specifically designed to tease apart these subprocesses. Participants compared externally presented face stimuli to a reference face held in WM, while alternating between updating and maintaining this reference, resulting in opening versus closing the gate to WM. Gate opening and substitution processes were associated with strong BG, thalamic, and frontoparietal activation, but intriguingly, the same activity profile was observed for sensory cortex supporting task stimulus processing (i.e., the fusiform face area). In contrast, gate closing was not reliably associated with any of these regions. These findings provide new support for the involvement of the BG in gate opening, as suggested by the gating model, but qualify the model's assumptions by demonstrating that gate closing does not seem to depend on the BG and that gate opening also involves task-relevant sensory cortex.