Although the default mode network (DMN) is associated with off-task states, recent evidence shows it can support tasks. This raises the question of how DMN activity can be both beneficial and detrimental to task performance. The decoupling hypothesis proposes that these opposing states occur because DMN supports modes of cognition driven by external input, as well as retrieval states unrelated to input. To test this account, we capitalised on the fact that during reading, regions in DMN are thought to represent the meaning of words through their coupling with visual cortex; the absence of visual coupling should occur when the attention drifts off from the text. We examined individual differences in reading comprehension and off-task thought while participants read an expository text in the laboratory, and related variation in these measures to (i) the neural response during reading in the scanner (Experiment 1), and (ii) patterns of intrinsic connectivity measured in the absence of a task (Experiment 2). The responsiveness of a region of DMN in middle temporal gyrus (MTG) to orthographic inputs during reading predicted good comprehension, while intrinsic decoupling of the same site from visual cortex at rest predicted more frequent off-task thought. In addition, good comprehension was associated with greater intrinsic connectivity between MTG and medial prefrontal regions also within DMN, demonstrating that DMN coupling can support task performance, not only off-task states. These findings indicate that the opposing roles of DMN in cognition reflect its capacity to support both perceptually-coupled and decoupled cognition.