The functional network of the brain continually adapts to changing environmental demands. The consequence of behavioral automation for task-related functional network architecture remains far from understood. We investigated the neural reflections of behavioral automation as participants mastered a dual n-back task. In four fMRI scans equally spanning a 6-week training period, we assessed brain network modularity, a substrate for adaptation in biological systems. We found that whole-brain modularity steadily increased during training for both conditions of the dual n-back task. In a dynamic analysis,we found that the autonomy of the default mode system and integration among task-positive systems were modulated by training. The automation of the n-back task through training resulted in non-linear changes in integration between the fronto-parietal and default mode systems, and integration with the subcortical system. Our findings suggest that the automation of a cognitively demanding task may result in more segregated network organization.