Chloroplasts of maize leaves differentiate into specific bundle sheath (BS) and mesophyll (M) types to accommodate C4 photosynthesis. Chloroplasts contain thylakoid and envelope membranes which contain the photosynthetic machineries and transporters, but also proteins involved in e.g. protein homeostasis. These chloroplast membranes must be specialized within each cell type to accommodate C4 photosynthesis and regulate metabolic fluxes and activities. This quantitative study determines the differentiated state of BS and M chloroplast thylakoid and envelope membrane proteomes and their oligomeric states, using innovative gel-based and mass spectrometry based protein quantifications. This includes native gels, iTRAQ and label-free quantification using a LTQ-Orbitrap. Subunits of Photosystem I, II, the cytochrome b6f and ATP-synthase complexes showed average BS/M accumulation ratios of respectively 1.6, 0.45, 1.0, 1.33, while ratios for the LCHI and the LHCII families were respectively 1.72 and 0.68. A 1000 kDa BS specific NDH complex with associated proteins of unknown function containing more than 15 proteins were observed; we speculate that this novel complex possibly functions in inorganic carbon concentration when carboxylation rates by Rubisco are lower than decarboxylation rates by malic enzyme. Differential accumulation of thylakoid proteases (Egy, DegP), state transition kinases (STN7,8) and PSII and PSI assembly factors was observed, suggesting that cell-specific photosynthetic electron transport depends on post-translational regulatory mechanisms. BS/M ratios for inner envelope transporters PPT, Dit1, Dit2 and Mex1 were determined and reflect metabolic fluxes in carbon metabolism. A wide variety of hundreds of other proteins showed differential BS/M accumulation. Mass spectral information and functional annotations are available through the Plant Proteome DataBase. These data are integrated with previous data, resulting in a model for C4 photosynthesis, thereby providing new rationales for metabolic engineering of C4 pathways and targeted analysis of genetic networks that coordinate C4 differentiation.