Photosystem II (PSII) and its associated light-harvesting complex II (LHCII) are highly concentrated in the stacked grana regions of photosynthetic thylakoid membranes from plants and green algae. PSII-LHCII supercomplexes can be arranged in disordered packings, ordered arrays, or mixtures thereof. The physical driving forces underlying array formation are unknown, and statistically robust methods of identifying arrays in micrographs are lacking, complicating attempts to determine a possible functional role for arrays in regulating light harvesting or energy conversion efficiency. This dissertation introduces new computational tools for studying the nano- and mesoscale organization of the membrane proteins that comprise the photosynthetic apparatus, and applies them to illuminate the origins of the diversity of local structural motifs in this adaptive biomaterial. First, we introduce a coarse-grained model of protein interactions in coupled photosynthetic membranes, focusing on a small number of particle types that feature simple shapes and potential energies motivated by structural studies. Reporting on computer simulations of the model's equilibrium fluctuations, we demonstrate its success in reproducing diverse structural features observed in experiments, including extended PSII-LHCII arrays. Free energy calculations reveal that the appearance of arrays marks a phase transition from the disordered fluid state to a system-spanning crystal. The predicted region of fluid-crystal coexistence is broad, encompassing much of the physiologically relevant parameter regime. Our results suggest that grana membranes lie at or near phase coexistence, conferring significant structural and functional flexibility to this densely packed membrane protein system. Upon extending this model to include simple representations of the membrane morphology and protein components found in thylakoid margins and stroma lamellae, we find that LHCII stacking and crowding in the grana are also primary determinants of the segregation of protein components between stacked and unstacked regions of the thylakoid membrane. In addition, we develop a statistical pipeline for identifying PSII crystals in nanometer-resolution micrographs of thylakoid membranes that would assist in future experimental tests of the predictions put forth in this dissertation; we validate our method on atomic force microscopy measurements of grana membranes isolated from Arabidopsis thaliana wild-type and soq1 mutant plants. As a whole, this work creates a foundation for future rigorous biophysical investigations of the structure, function, and dynamics of the photosynthetic apparatus.