Rubisco activity is essential for all life on earth, capturing atmospheric CO2 and incorporating it into photosynthesis-driven metabolism. Cyanobacteria encapsulate rubisco into bacterial microcompartments called carboxysomes to elevate the local CO2 concentration and enhance rubisco kinetics. The permeability across carboxysome shells is a key parameter to understand the CO2 concentration mechanism in cyanobacteria, as it limits the concentration gradient between the inside and outside of the carboxysome. Through molecular simulation, we track the motion of photosynthetic metabolites across the synthetic carboxysome shell to determine a permeability coefficient, and further compare them to the rate of CO2 leakage and turnover within model carboxysomes. This mechanistic insight is paramount to design and engineer such organelles for carbon fixation, bioenergy, and sustainability applications. D.S., M.S., C.A.K. and J.V.V. conceptualized the study. D.S. designed, ran, and analyzed the molecular dynamics simulations, with supervision and support from J.V.V. D.S. and C.M. developed the Brownian dynamics models, with supervision and support from A.A. D.S. wrote the first draft of the manuscript, with all authors contributing revisions.