Multi-state metastability in neuroimaging signals reflects the brain’s flexibility to transition between network configurations in response to changing environments or tasks. We modeled these dynamics with a Kuramoto network of 90 nodes oscillating at an intrinsic frequency of 40 Hz, interconnected using human brain structural connectivity strengths and delays. We simulated this model for 30 min to generate multi-state metastability. We identified global coupling and delay parameters that maximize spectral entropy, a proxy for multi-state metastability. At this operational point, multiple frequency-specific coherent sub-networks spontaneously emerge across oscillatory modes, persisting for periods between 140 and 4300 ms, reflecting flexible and sustained dynamic states. The topography of these sub-networks aligns with empirical resting-state neuroimaging data. Additionally, periodic components of the EEG spectra from young healthy participants correlate with maximal multi-state metastability, while dynamics away from this point correlate with sleep and anesthesia spectra. Our findings suggest that multi-state metastable functional dynamics observed in empirical data emerge from specific interactions of structural topography and connection delays, providing a platform to study mechanisms underlying flexible dynamics of cognition.