The bathochromic shift (>0.5 eV) in the absorption spectrum of the carotenoid astaxanthin upon incorporation into crustacyanin proteins is investigated. Several previously suggested explanations are tested and assessed by direct comparison to experimental absorption and circular dichroism spectra. We investigate the effect of extended models for the protein binding pocket, which results in only small contributions to the total shift. The possible explanation in terms of protonated histidine residues interacting with the astaxanthin molecules is analyzed by calculation of nuclear magnetic resonance chemical shifts. The results indicate that such a protonation is unlikely. In addition, we show that excitonic couplings are too weak to explain the red shift in the absorption spectrum, but the resulting intensity distribution actually leads to a blue shift of the major absorption peak. These findings are corroborated by a comparison of the theoretical and experimental circular dichroism spectra. We analyze changes in the relative orientation of the two astaxanthin molecules present in β-crustacyanin, which may lead to increased excitonic coupling and modified intensity distributions.