At rest, mammalian brains display a rich complex spatiotemporal behavior, which is reminiscent of healthy brain function and has provided nuanced understandings of several major neurological conditions. Despite the increasingly detailed phenomenological documentation of the brain’s resting state, its principle underlying causes remain unknown. To establish causality, we link structurally defined features of a brain network model to neural activation patterns and their variability. For the mouse, we use a detailed connectome-based model and simulate the resting state dynamics for neural sources and whole brain imaging signals (Blood-Oxygen-Level-Dependent (BOLD), Electroencephalography (EEG)). Under conditions of near-criticality, characteristic neuronal cascades form spontaneously and propagate through the network. The largest neuronal cascades produce short-lived but robust co-fluctuations at pairs of regions across the brain. During these co-activation episodes, long-lasting functional networks emerge giving rise to epochs of stable resting state networks correlated in time. Sets of neural cascades are typical for a resting state network, but different across. We experimentally confirm the existence and stability of functional connectivity epochs comprising BOLD co-activation bursts in mice (N=19). We further demonstrate the leading role of the neuronal cascades in a simultaneous EEG/fMRI data set in humans (N=15), explaining a large part of the variability of functional connectivity dynamics. We conclude that short-lived neuronal cascades are a major robust dynamic component contributing to the organization of the slowly evolving spontaneous fluctuations in brain dynamics at rest.