A fundamental question in systems neuroscience is how endogenous neuronal activity self-organizes during particular brain states. Recent neuroimaging studies have revealed systematic relationships between resting-state and task-induced functional connectivity (FC). In particular, continuous task studies, such as movie watching, speak to alterations in coupling among cortical regions and enhanced fluctuations in FC compared to resting-state. This suggests that FC may reflect systematic and large-scale reorganization of functionally integrated responses while subjects are watching movies. In this study, we characterized fluctuations in FC during resting-state and movie-watching conditions. We found that the FC patterns induced systematically by movie-watching can be explained with a single principal component. These condition-specific FC fluctuations overlapped with inter-subject synchronization patterns in occipital and temporal brain regions. However, unlike inter-subject synchronization, condition-specific FC patterns contained increased correlations within frontal brain regions and reduced correlations between frontal-parietal brain regions. We investigated the condition-specific functional variations as a shorter time scale, using time-resolved FC. The time-resolved FC showed condition-specificity over time, notably when subjects were also watching the same and different movie scenes. To explain the self-organisation of whole-brain FC through the alterations in local dynamics, we used a large-scale computational model. We found that the condition-specific reorganization of FC could be explained by local changes that engendered changes in FC among higher-order association regions, mainly in frontal parietal cortices.