Our understanding about the functionality of the brain's default network (DN) has significantly evolved over the past decade. Whereas traditional views define this network based on its suspension/disengagement during task-oriented behavior, contemporary accounts have characterized various situations wherein the DN actively contributes to task performance. However, it is unclear how different task-contexts drive componential regions of the DN to coalesce into a unitary network and fractionate into different subnetworks. Here we report a compendium of evidence that provides answers to these questions. Across multiple analyses, we found a striking dyadic structure within the DN in terms of the profiles of task-triggered fMRI response and effective connectivity, significantly extending beyond previous inferences based on meta-analysis and resting-state activities. In this dichotomy, one subset of DN regions prefers mental activities "interfacing with" perceptible events, while the other subset prefers activities "detached from" perceptible events. While both show a common "aversion" to sensory-motoric activities, their differential preferences manifest a subdivision that sheds light upon the taxonomy of the brain's memory systems. This dichotomy is consistent with proposals of a macroscale gradational structure spanning across the cerebrum. This gradient increases its representational complexity, from primitive sensory-motoric processing, through lexical-semantic representations, to elaborated self-generated thoughts.