In the absence of visual feedback, the perceived orientation of the fingers is systematically biased. In right-handers these biases are asymmetrical between the left and right hands in the horizontal plane and may reflect common functional postures for the two hands. Here we compared finger orientation perception in right- and left-handed participants for both hands, across various hand positions in the horizontal plane. Participants rotated a white line on a screen optically superimposed over their hand to indicate the perceived position of the finger that was rotated to one of seven orientations with the hand either aligned with the body midline, aligned with the shoulder, or displaced by twice the shoulder-to-midline distance from the midline. We replicated the asymmetric pattern of biases previously reported in right-handed participants (left hand biased towards an orientation ~30° inward, right hand ~10° inward). However, no such asymmetry was found for left-handers, suggesting left-handers may use different strategies when mapping proprioception to body or space coordinates and/or have less specialization of function between the hands. Both groups’ responses rotated further outward as distance of the hand from the body midline increased, consistent with other research showing spatial orientation estimates diverge outward in the periphery. Finally, for right-handers, precision of responses was best when the hand was aligned with the shoulder compared to the other two conditions. These results highlight the unique role of hand dominance and hand position in perception of finger orientation, and provide insight into the proprioceptive position sense of the upper limbs.