Vernier acuity has usually been tested with stimuli of the same contrast polarity (SC). This traditional vernier acuity was compared to that obtained with stimuli of opposite-contrast (OC) in which one target was brighter than the background and the other was darker. For both bar and dot targets vernier acuity with OC stimuli was about half as good as with SC stimuli. There were large individual differences in the size of the disadvantage with OC stimuli, although thresholds remained within the hyperacuity range. There were also individually-differing biases to see a dark vernier stimulus on one or the other side of a bright stimulus. Differences between OC and SC vernier acuities persisted over a wide range of interstimulus spacings, widths, and contrasts. At extremes of these spatial manipulations acuities became similar, but only because SC acuities were degraded to the level of OC acuities. Subjects showed little improvement in OC vernier acuity, even after 50,000 trials. It is concluded that finest judgements of spatial position arise in a level of the visual system at which light and dark stimuli are treated independently.