Background: The study of intrinsic connectivity networks, i.e., sets of brain regions that show a high degree of interconnectedness even in the absence of a task, showed that major depressive disorder (MDD) patients demonstrate an increased connectivity within the default mode network (DMN), which is active in a resting state and is implicated in self-referential processing, and a decreased connectivity in task-positive networks (TPNs), which increase their activity in attention tasks. Cortical localization of this ‘dominance’ of the DMN over the TPN in MDD patients is not fully understood. Besides, this effect has been investigated using fMRI and its electrophysiological underpinning is not known. Method: In this study, we tested the dominance hypothesis using seed-based connectivity analysis of resting-state fMRI and EEG data obtained in 41 MDD patients and 23 controls. Results: In MDD patients, as compared to controls, insula, pallidum/putamen, amygdala, and left dorso- and ventrolateral prefrontal cortex are more strongly connected with DMN than with TPN seeds. In EEG, all significant effects were obtained in the delta frequency band. Limitations: fMRI and EEG data were not obtained simultaneously during the same session. Conclusions: In MDD patients, major emotion and attention regulation circuits are more strongly connected with DMN than with TPN implying they are more prepared to respond to internally generated self-related thoughts than to environmental challenges.