The dim-light photoreceptor rhodopsin has been a structural model for G protein-coupled receptors (GPCRs) for decades, so much so that the largest class of GPCRs is commonly called “rhodopsin-like.” However, the visual receptor has several unique characteristics that differentiate it from other members of the superfamily. Most notably, rather than interacting through a diffusible ligand, the receptor covalently binds its light-sensitive inverse agonist, 11-cis retinal (11CR), which locks the complex in an “off” state. Activation occurs when the 11CR-rhodopsin complex absorbs light, and isomerizes the ligand into the agonist all-trans retinal (ATR). After activation, the ATR is exchanged for a fresh 11CR in order to reset the protein for further light detection. Therefore, despite the covalent nature of the retinal-rhodopsin interaction, the ligand must be capable of entering and exiting the receptor. So it may come as a surprise that, although rhodopsin was the first solved GPCR crystal structure, how the retinals bind and dissociate from the protein remains unanswered. This dissertation attempts to address this question.