The color vision of Old World primates and humans uses two cone-opponent systems; one differences the outputs of L and M cones forming a red–green (RG) system, and the other differences S cones with a combination of L and M cones forming a blue–yellow (BY) system. In this paper, we show that in human vision these two systems have a differential distribution across the visual field. Cone contrast sensitivities for sine-wave grating stimuli (smoothly enveloped in space and time) were measured for the two color systems (RG & BY) and the achromatic (Ach) system at a range of eccentricities in the nasal field (0–25 deg). We spatially scaled our stimuli independently for each system (RG, BY, & Ach) in order to activate that system optimally at each eccentricity. This controlled for any differential variations in spatial scale with eccentricity and provided a comparison between the three systems under equivalent conditions. We find that while red–green cone opponency has a steep decline away from the fovea, the loss in blue–yellow cone opponency is more gradual, showing a similar loss to that found for achromatic vision. Thus only red–green opponency, and not blue–yellow opponency, can be considered a foveal specialization of primate vision with an overrepresentation at the fovea. In addition, statistical calculations of the level of chance cone opponency in the two systems indicate that selective S cone connections to postreceptoral neurons are essential to maintain peripheral blue–yellow sensitivity in human vision. In the red–green system, an assumption of cone selectivity is not required to account for losses in peripheral sensitivity. Overall, these results provide behavioral evidence for functionally distinct neuro-architectural origins of the two color systems in human vision, supporting recent physiological results in primates.