Evolutionarily relevant networks have been previously described in several mammalian species using time-averaged analyses of fMRI time-series. However, fMRI network activity is highly dynamic and continually evolves over timescales of seconds. Whether the dynamic organization of resting-state fMRI network activity is conserved across mammalian species remains unclear. Using frame-wise clustering of fMRI time-series, we find that intrinsic fMRI network dynamics in awake macaques and humans is characterized by recurrent transitions between a set of 4 dominant, neuroanatomically homologous fMRI coactivation modes (C-modes), three of which are also plausibly represented in the rodent brain. Importantly, in all species C-modes exhibit species-invariant dynamic features, including preferred occurrence at specific phases of fMRI global signal fluctuations, and a state transition structure compatible with infraslow coupled oscillator dynamics. Moreover, dominant C-mode occurrence reconstitutes the static organization of the fMRI connectome in all species, and is predictive of ranking of corresponding fMRI connectivity gradients. These results reveal a set of species-invariant principles underlying the dynamic organization of fMRI networks in mammalian species, and offer novel opportunities to relate fMRI network findings across the phylogenetic tree.