Resting state functional connectivity has been promoted as a promising tool for creating cortical maps that show remarkable similarity to those established by invasive histological methods. While this tool has been largely used to identify and map cortical areas, its true potential in the context of studying connectional architecture and in conducting comparative neuroscience has remained unexplored. Here, we employ widely used resting state connectivity and data-driven clustering methods to extend this approach for the study of the organizational principles of the macaque parietal–frontal system. We show multiple, overlapping principles of organization, including a dissociation between dorsomedial and dorsolateral pathways and separate parietal–premotor and parietal–frontal pathways. These results demonstrate the suitability of this approach for understanding the complex organizational principles of the brain and for large-scale comparative neuroscience.