Goal-directed movements can fail due to errors in our perceptual and motor systems. While these errors may arise from random noise within these sources, they also reflect systematic motor biases that vary with the location of the target. The origin of these systematic biases remains controversial. Drawing on data from an extensive array of reaching tasks conducted over the past 30 years, we evaluated the merits of various computational models regarding the origin of motor biases. Contrary to previous theories, we show that motor biases do not arise from systematic errors associated with the sensed hand position during motor planning or from the biomechanical constraints imposed during motor execution. Rather, motor biases are primarily caused by a misalignment between eye-centric and the body-centric representations of position. This model can account for motor biases across a wide range of contexts, encompassing movements with the right versus left hand, proximal and distal effectors, visible and occluded starting positions, as well as before and after sensorimotor adaptation.