Moving objects generate motion information at different scales, which are processed in the visual system with a bank of spatiotemporal frequency channels. It is not known how the brain pools this information to reconstruct object speed and whether this pooling is generic or adaptive; that is, dependent on the behavioral task. We used rich textured motion stimuli of varying bandwidths to decipher how the human visual motion system computes object speed in different behavioral contexts. We found that, although a simple visuomotor behavior such as short-latency ocular following responses takes advantage of the full distribution of motion signals, perceptual speed discrimination is impaired for stimuli with large bandwidths. Such opposite dependencies can be explained by an adaptive gain control mechanism in which the divisive normalization pool is adjusted to meet the different constraints of perception and action.