Although brain changes associated with the acquisition of cognitive abilities in early childhood involve increasing localized specialization, little is known about the brain changes associated with the refinement of existing cognitive abilities that reach maturity in adolescence. The goal of this study was to investigate developmental changes in functional brain circuitry that support improvements in visuospatial working memory from childhood to adulthood. We tested thirty 8- to 47-year-olds in an oculomotor delayed response task. Developmental transitions in brain circuitry included both quantitative changes in the recruitment of necessary working memory regions and qualitative changes in the specific regions recruited into the functional working memory circuitry. Children recruited limited activation from core working memory regions (dorsal lateral prefrontal cortex [DLPFC] and parietal regions) and relied primarily on ventromedial regions (caudate nucleus and anterior insula). With adolescence emerged a more diffuse network (DLPFC, anterior cingulate, posterior parietal, anterior insula) that included the functional integration of premotor response preparation and execution circuitry. Finally, adults recruited the most specialized network of localized regions together with additional performance-enhancing regions, including left-lateralized DLPFC, ventrolateral prefrontal cortex, and supramarginal gyrus. These results suggest that the maturation of adult-level cognition involves a combination of increasing localization within necessary regions and their integration with performance-enhancing regions.