The brain's intrinsic functional architecture, revealed in correlated spontaneous activity, appears to constitute a faithful representation of its repertoire of evoked, extrinsic functional interactions. Here, using broad task contrasts to probe evoked patterns of coactivation, we demonstrate tight coupling between the brain's intrinsic and extrinsic functional architectures for default and task-positive regions, but not for subcortical and limbic regions or for primary sensory and motor cortices. While strong correspondence likely reflects persistent or recurrent patterns of evoked coactivation, weak correspondence may exist for regions whose patterns of evoked functional interactions are more adaptive and context dependent. These findings were independent of task. For tight task contrasts (e.g., incongruent vs. congruent trials), evoked patterns of coactivation were unrelated to the intrinsic functional architecture, suggesting that high-level task demands are accommodated by context-specific modulations of functional interactions. We conclude that intrinsic approaches provide only a partial understanding of the brain's functional architecture. Appreciating the full repertoire of dynamic neural responses will continue to require task-based functional magnetic resonance imaging approaches.