Recent laminar-fMRI studies have provided substantial understanding of the evoked cortical responses in multiple sub-systems; in contrast, the laminar component of resting-state networks remains largely unknown. Here, we used EPIK, which offers unprecedented coverage at sub-millimetre resolution, to investigate cortical resting-state dynamics with depth specificity. After verifying laminar activation profiles in response to a task, we investigated whole-brain laminar dynamics. During rest, signal oscillations were stronger in the superficial layers of the cortical ribbon, and functional connectivity analysis indicated that most resting-state cortical connections occurring at rest involve supra-granular layers. Coherence assessed in a lateral motor network suggested a modified distribution of layer-specific responses during task performance compared to resting-state. Whole-brain evaluation of laminar-fMRI encompasses unprecedented computational challenges; nonetheless, it enables a new dimension of the human cerebral cortex to be investigated from a global view, which may be key in the characterization of neurological disorders from a novel perspective.Significance statementResting-state networks sustain conscious awareness and diverse cognitive processing in the absence of tasks. In contrast to cortical areas, the cortical depth-specific signals across different networks have been poorly investigated, mainly due to the small brain coverage enforced in high-resolution imaging methods. Here, we demonstrate the different involvement of the cortical layers in the maintenance of the resting-state dynamics at near whole-brain level, using an optimized fMRI sequence. Given the cytoarchitectonics of the human neocortex, and based on our results, the cortical thickness constitutes an important dimension to characterize the resting-state oscillations in the healthy brain and its functional study may facilitate the identification of novel targets in neurological diseases.