To determine the direction of object motion in external space, the brain must combine retinal motion signals and information about the orientation of the eyes in space. We assessed the accuracy of this process in eight laterally tilted subjects who aligned the motion direction of a random-dot pattern (30% coherence, moving at 6 degrees /s) with their perceived direction of gravity (motion vertical) in otherwise complete darkness. For comparison, we also tested the ability to align an adjustable visual line (12 degrees diameter) to the direction of gravity (line vertical). For small head tilts (<40 degrees ), systematic errors in either task were almost negligible. In contrast, tilts >60 degrees revealed a pattern of large systematic errors (often >30 degrees ) that was virtually identical in both tasks. Regression analysis confirmed that mean errors in the two tasks were closely related, with slopes close to 1.0 and correlations >0.89. Control experiments ruled out that motion settings were based on processing of individual single-dot paths. We conclude that the conversion of both motion direction and line orientation on the retina into a spatial frame of reference involves a shared computational strategy. Simulations with two spatial-orientation models suggest that the pattern of systematic errors may be the downside of an optimal strategy for dealing with imperfections in the tilt signal that is implemented before the reference-frame transformation.