Trichromacy in humans and other Old World primates evolved from a dichromatic color vision system ≈30–40 million years ago. One essential part of this evolution was the duplication and divergence of sequences on the X chromosome to create the present-day red and green cone pigment genes. Earlier work demonstrated that a locus control region (LCR) located upstream of these genes is essential for their expression. In the present work, we have generated a variety of modified human red and green pigment gene arrays that direct the expression of distinguishable histochemical reporters from each gene promoter. Transgenic mice carrying a single copy of each modified array were studied to define the role of three variables in producing mutually exclusive expression of red and green pigment transgenes: the distance between the promoter and the LCR, the identity of the visual pigment promoter, and LCR copy number. The results support a model in which the mutually exclusive expression of these genes in their respective cone types is controlled by competition between visual pigment promoters for pairing with the LCR, and they suggest a facile mechanism for the evolution of trichromacy after visual pigment gene duplication.