Complex brain function comprises a multitude of neural operations in parallel and often at different speeds. Each of these operations is carried out across a network of distributed brain regions. How multiple distributed processes are facilitated in parallel is largely unknown. We postulate that such processing relies on a multiplex of dynamic network patterns emerging in parallel but from different functional connectivity (FC) timescales. Given the dominance of inherently slow fMRI in network science, it is unknown whether the brain leverages such multi-timescale network dynamics. We studied FC dynamics concurrently across a breadth of timescales (from infraslow to γ-range) in rare, simultaneously recorded intracranial EEG and fMRI in humans, and source-localized scalp EEG-fMRI data in humans. We examined spatial and temporal convergence of connectome trajectories across timescales. ‘Spatial convergence’ refers to spatially similar EEG and fMRI connectome patterns, while ‘temporal convergence’ signifies the more specific case of spatial convergence at corresponding timepoints in EEG and fMRI. We observed spatial convergence but temporal divergence across FC timescales; connectome states (recurrent FC patterns) with partial spatial similarity were found in fMRI and all EEG frequency bands, but these occurred asynchronously across FC timescales. Our findings suggest that hemodynamic and frequency-specific electrophysiological signals, while involving similar large-scale networks, represent functionally distinct connectome trajectories that operate at different FC speeds and in parallel. This multiplex is poised to enable concurrent connectivity across multiple sets of brain regions independently.