Accurate characterization of the spatiotemporal relationship between two of the most prominent neuroimaging measures of neuronal activity, the 8–13 Hz, occipito-parietal EEG alpha oscillation and the BOLD fMRI signal, must encompass the intrinsically dynamic nature of both alpha power and brain function. Here, during the eyes-open resting state, we use a 16 s sliding-window analysis and demonstrate that the mean spatial network of dynamic alpha-BOLD correlations is highly comparable to the static network calculated over six minutes. However, alpha-BOLD correlations showed substantial spatiotemporal variability within-subjects and passed through many different configurations such that the static network was fully represented in only ~10% of 16 s epochs, with visual and parietal regions (coherent on average) often opposingly correlated with each other or with alpha. We find that the common assumption of static-alpha BOLD correlations greatly oversimplifies temporal variation in brain network dynamics. Fluctuations in alpha-BOLD coupling significantly depended upon the instantaneous amplitude of alpha power, and primary and lateral visual areas were most strongly negatively correlated with alpha during different alpha power states, possibly suggesting the action of multiple alpha mechanisms. Dynamic alpha-BOLD correlations could not be explained by eye-blinks/movements, head motion or non-neuronal physiological variability. Individual's mean alpha power and frequency were found to contribute to between-subject variability in alpha-BOLD correlations. Additionally, application to a visual stimulation dataset showed that dynamic alpha-BOLD correlations provided functional information pertaining to the brain's response to stimulation by exhibiting spatiotemporal fluctuations related to variability in the trial-by-trial BOLD response magnitude. Significantly weaker visual alpha-BOLD correlations were found both preceding and following small amplitude BOLD response trials compared to large response trials.