The human brain is a dynamic modular network that can be decomposed into a set of modules, and its activity changes continually over time. At rest, several brain networks, known as Resting-State Networks (RSNs), emerge and cross-communicate even at sub-second temporal scale. Here, we seek to decipher the fast reshaping in spontaneous brain modularity and its relationships with RSNs. We use Electro/Magneto-Encephalography (EEG/MEG) to track the dynamics of modular brain networks, in three independent datasets (N = 568) of healthy subjects at rest. We show the presence of strikingly consistent RSNs, and a splitting phenomenon of some of these networks, especially the default mode network, visual, temporal and dorsal attentional networks. We also demonstrate that between-subjects variability in mental imagery is associated with the temporal characteristics of specific modules, particularly the visual network. Taken together, our findings show that large-scale electrophysiological networks have modularity-dependent dynamic fingerprints at rest.