Computational models that predict the spectral sensitivities of primate cone photoreceptors have focussed only on the spectral, not spatial, dimensions. On the ecologically valid task of foraging for fruit, such models predict the M-cone (“green”) peak spectral sensitivity 10–20 nm further from the L-cone (“red”) sensitivity peak than it is in nature and assume their separation is limited by other visual constraints, such as the requirement of high-acuity spatial vision for closer M and L peak sensitivities. We explore the possibility that a spatio-chromatic analysis can better predict cone spectral tuning without appealing to other visual constraints. We build a computational model of the primate retina and simulate chromatic gratings of varying spatial frequencies using measured spectra. We then implement the case study of foveal processing in routinely trichromatic primates for the task of discriminating fruit and leaf spectra. We perform an exhaustive search for the configurations of M and L cone spectral sensitivities that optimally distinguish the colour patterns within these spectral images. Under such conditions, the model suggests that: (1) a long-wavelength limit is required to constrain the L cone spectral sensitivity to its natural position; (2) the optimal M cone peak spectral sensitivity occurs at ~525 nm, close to the observed position in nature (~535 nm); (3) spatial frequency has a small effect upon the spectral tuning of the cones; (4) a selective pressure toward less correlated M and L spectral sensitivities is provided by the need to reduce noise caused by the luminance variation that occurs in natural scenes.