The functional network of the human brain continually adapts to changing environmental demands. Such adaptation spans multiple time scales, from seconds during task performance to days and weeks during motor or cognitive training. Yet the precise consequence of behavioral automation for functional network architecture, particularly in the context of complex tasks, remains far from understood. Here we investigated the neural reflections of behavioral adaptation as human participants mastered a dual n-back task over 6 weeks of training. In four fMRI scans equally spanning the training period, we assessed the level of brain network modularity, a common substrate for adaptation in biological systems. Specifically, we investigated both static and dynamic modularity to probe the segregation between task-relevant fronto-parietal and default mode systems, and to assess their time-evolving recruitment and integration. We found that whole-brain modularity was higher during the resting state than during the dual n-back task, and increased as demands heightened from the 1-back to the 2-back condition. Modularity also steadily increased in response to training for both task conditions. In an explicitly dynamic analysis, we found that the recruitment of both the default mode and fronto-parietal systems during the dual n-back task was modulated by training. Moreover, the change in default mode recruitment from the first scanning session to the last was positively correlated with behavioral improvement after training. Reliably across static and dynamic network analyses, our findings suggest that the automation of a cognitively demanding task may result in more segregated network organization.