Working memory (WM), the short-term abstraction and manipulation of information, is an essential neurocognitive process in daily functioning. Few studies have concurrently examined the functional and structural neural correlates of WM and the current study did so to characterize both overlapping and unique associations. Participants were a large sample of adults from the Human Connectome Project (N = 1064; 54% female) who completed an in-scanner visual N-back WM task. The results indicate a clear dissociation between BOLD activation during the WM task and brain structure in relation to performance. In particular, while activation in the middle frontal gyrus was positively associated with WM performance, cortical thickness in this region was inversely associated with performance. Additional unique associations with WM were BOLD activation in superior parietal lobule, cingulate, and fusiform gyrus and gray matter volume in the orbitofrontal cortex and cuneus. Across findings, substantially larger effects were observed for functional associations relative to structural associations. These results provide further evidence implicating frontoparietal subunits of the brain in WM. Moreover, these findings reveal the distinct, and in some cases opposing, roles of brain structure and neural activation in WM, highlighting the lack of homology between structure and function in relation to cognition.