Spontaneous brain activity is organized into resting-state networks (RSNs) involved in internally-guided, higher-order mental functions (default mode, central executive and salience networks) and externally-driven, specialized sensory and motor processing (auditory, visual and sensorimotor networks). RSNs are characterized by their functional connectivity in terms of within-network cohesion and between-network integration, and by their dynamic properties in terms of synchrony and metastability. We examined the relationship between functional connectivity and dynamic network features using fMRI data and an anatomically constrained Kuramoto model. Extrapolating from simulated data, synchrony and metastability across the RSNs emerged at coupling strengths of 5 ≤ k ≤ 12. In the empirical RSNs, higher metastability and synchrony were respectively associated with greater cohesion and lower integration. Consistent with their dual role in supporting both sustained and diverse mental operations, higher-order RSNs had lower metastability and synchrony. Sensory and motor RSNs showed greater cohesion and metastability, likely to respectively reflect their functional specialization and their greater capacity for altering network states in response to multiple and diverse external demands. Our findings suggest that functional and dynamic RSN properties are closely linked and expand our understanding of the neural architectures that support optimal brain function.