Cognition is dynamic, allowing us the flexibility to shift focus from different aspects of the environment, or between internally- and externally-oriented trains of thought. Although we understand how individuals switch attention across different tasks, the neurocognitive processes that underpin the dynamics of less constrained elements of cognition are less well understood. To explore this issue, we developed a paradigm in which participants intermittently responded to external events across two conditions that systematically vary in their need for updating working memory based on information in the external environment. This paradigm distinguishes the influences on cognition that emerge because of demands placed by the task (sustained) from changes that result from the time elapsed since the last task response (transient). We used experience sampling to identify dynamic changes in ongoing cognition in this paradigm, and related between subject variation in these measures to variations in the intrinsic organisation of large-scale brain networks. We found systems important for attention were involved in the regulation of off-task thought. Coupling between the ventral attention network and regions of primary motor cortex was stronger for individuals who were able to regulate off-task thought in line with the demands of the task. This pattern of coupling was linked to greater task-related thought when environmental demands were high and elevated off-task thought when demands were low. In contrast, the coupling of the dorsal attention network with a region of lateral visual cortex was stronger for individuals for whom off-task thoughts transiently increased with the time since responding to the external world increased. This pattern is consistent with a role for this system in the time-limited top-down biasing of visual processing to increase behavioural efficiency. Unlike the attention networks, coupling between regions of the default mode network and dorsal occipital cortex was weaker for individuals for whom the level of detail decreased with the passage of time when the external task did not require continuous monitoring of external information. These data provide novel evidence for how neural systems vary across subjects and may be underpin individual variation in the dynamics of thought, linking attention systems to the maintenance of task-relevant information, and the default mode network to supporting experiences with vivid detail.