Consciousness emerges from the spatiotemporal dynamics of neural activity. However, how such an extraordinary phenomenon is supported by neural flexibility and regional specialization across the cerebral cortex remains elusive. Here, using several functional magnetic resonance imaging (fMRI) paradigms (e.g., anesthesia, sleep, and drowsiness), we show a consciousness-related signature characterized by shifting spontaneous fluctuations along a unimodal-transmodal cortical organizational axis. The signature is simple and sensitive to altered states of consciousness in single individuals, exhibiting abnormal elevation under psychedelics as well as in individuals with psychosis. Under task-free conditions, this hierarchical dynamic reflects ongoing brain state changes in global integration and connectome diversity. Applying quasi-periodic pattern detection during different vigilance states, we found that hierarchical heterogeneity also manifested as spatiotemporally propagation waves related to arousal. A similar pattern was observed in neural activity measured with cortex-wide electrocorticography (ECoG) in macaques. Last, we observed that the spatial distribution of the principle cortical gradient not only preferentially recapitulated the genetic transcription levels of the histaminergic system but also that of the functional connectome mapping of the tuberomammillary nucleus (TMN), which promotes wakefulness. Combining behavioral, neuroimaging, electrophysiological, and transcriptomic evidence, we suggest that global state of consciousness is supported by efficient hierarchical processing that can be constrained along a low-dimensional macroscale gradient.