Typical linear and porphyrin-like structure representations of bilirubin give an incorrect impression of its actual shape and expected solution properties. Conformational analysis of bilirubin, assisted by molecular dynamics computations, indicates that (i) nonbonded intramolecular steric interactions are minimized in a ridge-tile shape conformation lying at a global energy minimum on the conformational energy map and (ii) considerable additional stabilization is achieved through a network of intramolecular hydrogenbonds. The linear and porphyrin-like conformations are computed to lie some 37-48 kcal/mol above the isoenergetic global minimum energy conformations, which correspond to superimposable (identical) or to nonsuperimposable (enantiomeric) mirror image intramolecularly hydrogen-bonded ridge-tile conformers. Two different low-energy (19.5 and 21.4 kcal/mol) transition states can be identified on pathways for interconverting these conformational enantiomers. The conformation of bilirubin may be determined experimentally by UV-visible and, especially, circular dichroism (CD) spectroscopy. Such conformation dependent spectra arise from exciton coupling between the two dipyrrinone chromophores of bilirubin. Theoretical analysis using the exciton coupled oscillator model allowed a mapping of CD DELTAepsilon for each bilirubin conformation of the conformational energy surface. An intense bisignate CD spectrum is predicted for the global energy minimum conformation with Cotton effects DELTAepsilon congruent-to +/-200 L mol-1 cm-1 for the long wavelength UV-visible absorption near 450 nm. Surprisingly, Cotton effect sign reversals without inversion of molecular absolute configuration are predicted when the ridge-tile conformations are flattened somewhat into higher energy structures.