We investigated the interaction between extra-retinal rotation signals and retinal motion signals in heading perception during pursuit eye movement. For limited viewing aperture, the variability in perceived heading strongly depends on the pattern of motion directions. Heading towards a point outside the aperture generates nearly parallel aperture flow. This results in lower precision of perceived heading than heading that renders the radial pattern of flow visible. We ask if the precision is limited by the pattern of flow visible on the retina or that on the screen. During fixation, the two patterns are identical. They are decoupled during pursuit, since pursuit changes radial flow within the aperture on the screen into nearly parallel flow on the retina, and vice versa. The extra-retinal signal is known to reduce systematic errors in the direction of pursuit, thus compensating for the rotational flow during pursuit. We now ask if the extra-retinal signal also affects the precision of heading percepts. It might if at the spatial integration stage the rotational flow has been subtracted out already. A compensation beyond the integration stage, however, cannot undo the change in retinal motion directions so that an effect of pursuit on precision cannot be avoided. We measured the variable and systematic errors in perceived heading during fixation and pursuit for a frontal plane approach, while varying duration, dot lifetime and aperture size. We found precision is effected by pursuit as much as predicted from the pattern of retinal flow, while compensation is significantly greater than zero. This means that the interaction between the extra-retinal signal and visual motion signals takes place after spatial integration of local motion signals. Furthermore, compensation increased significantly with longer duration (0.5–3.0 s), but not with larger aperture size (10–50°). A larger aperture size did increase the eccentricity of perceived heading.