Cognitive function evolves significantly over development, enabling flexible control of human behavior. Yet, how these functions are instantiated in spatially distributed and dynamically interacting networks, or graphs, that change in structure from childhood to adolescence is far from understood. Here we applied a novel machine-learning method to track continuously overlapping and time-varying subgraphs in the brain at rest within a sample of 200 healthy youth (ages 8–11 and 19–22) drawn from the Philadelphia Neurodevelopmental Cohort. We uncovered a set of subgraphs that capture surprisingly integrated and dynamically changing interactions among known cognitive systems. We observed that subgraphs that were highly expressed were especially transient, flexibly switching between high and low expression over time. This transience was particularly salient in a subgraph predominantly linking frontoparietal regions of the executive system, which increases in both expression and flexibility from childhood to young adulthood. Collectively, these results suggest that healthy development is accompanied by an increasing precedence of executive networks and a greater switching of the regions and interactions subserving these networks. Abstract AUTHOR SUMMARY Our ability to thoughtfully engage with the world around us changes appreciably as we transition from childhood to adulthood. Yet, how our brains develop to enable that change remains far from understood. Here we used network science—traditionally applied to the study of social networks like Facebook or Twitter—and machine learning to show that growing cognitive abilities are accompanied by greater flexibility of brain regions within distributed networks. This flexibility is greatest in the executive system, which is critical for higher-order cognitive functions and increases in expression and flexibility from childhood to young adulthood. These results suggest that healthy development is facilitated by an increasing precedence of executive networks and a greater switching of the regions and interactions subserving these networks.