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Understanding the functions of multi‐cellular organs in terms of the molecular networks within each cell is an important step in the quest to predict phenotype from genotype. B‐lymphocyte population dynamics, which are predictive of immune response and vaccine effectiveness, are determined by individual cells undergoing division or death seemingly stochastically. Based on tracking single‐cell time‐lapse trajectories of hundreds of B cells, single‐cell transcriptome, and immunofluorescence analyses, we constructed an agent‐based multi‐modular computational model to simulate lymphocyte population dynamics in terms of the molecular networks that control NF‐κB signaling, the cell cycle, and apoptosis. Combining modeling and experimentation, we found that NF‐κB cRel enforces the execution of a cellular decision between mutually exclusive fates by promoting survival in growing cells. But as cRel …