Behavioral evidence suggests that different mechanisms mediate duration perception depending on whether regular or irregular cues for time estimation are provided, and that individual differences in interoceptive processing may affect duration perception only in the latter case. However, no study has addressed brain correlates of this proposed distinction. Here participants performed a duration reproduction task in two conditions: with unevenly spaced stimuli during time estimation/reproduction (irregular), with regularly spaced stimuli provided during the same task (regular). They also underwent resting-state fMRI to assess regional functional connectivity, in order to link individual differences in behavioral performance to variations in patterns of intrinsic brain oscillations. Resting-state functional connectivity of the right precentral gyrus with the ipsilateral insula and putamen was predicted by duration reproduction performance selectively in the irregular condition. The connectivity of the right posterior insula, within a network modulated by participants’ degree of interoceptive awareness, correlated positively with performance in the irregular condition only. Findings support the distinction between brain networks involved in duration processing with or without regular cues, and the hypothesis that the multimodal integration of interoceptive and exteroceptive cues is specifically involved in the latter.