We present a structure-based theory of the long-wavelength (red/green) color tuning in visual rhodopsins and its application to the analysis of site-directed mutagenesis experiments. Using a combination of electrostatic and molecular-mechanics methods, we explain the measured mutant-minus-wild-type absorption shifts and conclude that the dominant mechanism of the color tuning in these systems is electrostatic pigment protein coupling. An important element of our analysis is the independent determination of protonation states of titratable residues in the wild type and the mutant protein as well as the self-consistent reoptimization of hydrogen atom positions, which includes the relaxation of the hydrogen bonding network and the reorientation of water molecules. On the basis of this analysis, we propose a "dipole orientation rule" according to which both the position and the orientation of a polar group introduced in the protein environment determine the direction of the transition energy shift of the retinal chromophore.