The animal brain is endowed with an innate sense of number allowing to intuitively perceive the approximate quantity of items in a scene, or “numerosity.” This ability is not limited to items distributed in space, but also to events unfolding in time and to the average numerosity of dynamic scenes. How the brain computes and represents the average numerosity over time, however, remains unclear. Here, we investigate the mechanisms and EEG signature of the perception of average numerosity over time. To do so, we used stimuli composed of a variable number (3–12) of briefly presented dot arrays (50 msec each) and asked participants to judge the average numerosity of the sequence. We first show that the weight of different portions of the stimuli in determining the judgment depends on how many arrays are included in the sequence itself: the longer the sequence, the lower the weight of the latest arrays. Second, we show systematic adaptation effects across stimuli in consecutive trials. Importantly, the EEG results highlight two processing stages whereby the amplitude of occipital ERPs reflects the adaptation effect (∼300 msec after stimulus onset) and the accuracy and precision of average numerosity judgments (∼450–700 msec). These two stages are consistent with processes involved with the representation of perceived average numerosity and with perceptual decision-making, respectively. Overall, our findings provide new evidence showing how the visual system computes the average numerosity of dynamic visual stimuli, and support the existence of a dedicated, relatively low-level perceptual mechanism mediating this process.