Chromophoric biomolecules are exploited as reporters of a diverse set of phenomena, acting as internal distance monitors, environment and redox sensors, and endogenous imaging probes. The extent to which they can be exploited is dependent on an accurate knowledge of their fundamental electronic properties. Arguably of greatest importance is a precise knowledge of the direction(s) of the absorption transition dipole moment(s) (TDMs) in the molecular frame of reference. Such is the case for flavins, fluorescent redox cofactors utilized for ground- and excited-state redox and photochemical processes. The directions of the TDMs in oxidized and semiquinone flavins were characterized decades ago, and the details of charge redistribution in these forms have also been studied by Stark spectroscopy. The electronic structure of the fully reduced hydroquinone anionic state, FlH(-), however, has been the subject of unfounded assumptions and estimates about the number and direction of TDMs in FlH(-), as well the electronic structure changes that occur upon light absorption. Here we have used Stark spectroscopy to measure the magnitude and direction of charge redistribution in FlH(-) upon optical excitation. These data were analyzed using TD-DFT calculations. The results show unequivocally that not one but two nearly orientation-degenerate electronic transitions are required to explain the 340-500 nm absorption spectral range, demolishing the commonly held assumption of a single transition. The difference dipole moments for these states show that electron density shifts toward the xylene ring for both transitions. These measurements force a reappraisal of previous studies that have used erroneous assumptions and unsubstantiated estimates of these quantities. The results put future optical studies of reduced flavins/flavoproteins on a firm photophysical footing.