Spontaneous brain activity as assessed with resting-state fMRI exhibits rich spatiotemporal structure. However, the principles by which brain-wide patterns of spontaneous fMRI activity reconfigure and interact with each other remain unclear. We used a framewise clustering approach to map spatiotemporal dynamics of spontaneous fMRI activity with voxel resolution in the resting mouse brain. We show that brain-wide patterns of fMRI co-activation can be reliably mapped at the group and subject level, defining a restricted set of recurring brain states characterized by rich network structure. Importantly, we document that the identified fMRI states exhibit contrasting patterns of functional activity and coupled infraslow network dynamics, with each network state occurring at specific phases of global fMRI signal fluctuations. Finally, we show that autism-associated genetic alterations entail the engagement of atypical functional states and altered infraslow network dynamics. Our results reveal a novel set of fundamental principles guiding the spatiotemporal organization of resting-state fMRI activity and its disruption in brain disorders.