Humans spend a large proportion of their time engaged in thoughts unrelated to the task being performed, a tendency that declines with age. However, a clear neuro-cognitive account of what underlies this decrease is lacking. This study addresses the possibility that age-related changes in off-task thinking are correlated with changes in the intrinsic organisation of the brain. Laboratory measures of ongoing thought were recorded in young and older individuals, who also participated in a resting state fMRI experiment. Older individuals showed reduced connectivity between the left anterior temporal lobe with prefrontal aspects of the DMN. We found that off-task thinking did not increase when task demands were lower for older adults, which is a pattern repeatedly seen in younger individuals. Finally, we demonstrated that these neural and thought patterns were linked – for younger participants only, reductions in the strength of connectivity were related to a greater shift towards off-task thoughts when task demands decreased. Importantly, in the older individuals, lower connectivity between the same regions was linked to preserved performance on a creativity task. These data suggest that the age-related reduction of off-task thought may be related to reduced communication between temporal and prefrontal DMN regions in ageing.