Present phytoplankton models typically use a population-level (lumped) modeling (PLM) approach that assumes average properties of a population within a control volume. For modern biogeochemical models that formulate growth as a nonlinear function of the internal nutrient (e.g. Droop kinetics), this averaging assumption can introduce a significant error. Individual-based (agent-based) modeling (IBM) does not make the assumption of average properties and therefore constitutes a promising alternative for biogeochemical modeling. This paper explores the hypothesis that the cell quota (Droop) model, which predicts the population-average specific growth or cell division rate, based on the population-average nutrient cell quota, can be applied to individual algal cells and produce the same population-level results. Three models that translate the growth rate calculated using the cell quota model into discrete cell division events are evaluated, including a stochastic model based on the probability of cell division, a deterministic model based on the maturation velocity and fraction of the cell cycle completed (maturity fraction), and a deterministic model based on biomass (carbon) growth and cell size. The division models are integrated into an IBM framework (iAlgae), which combines a lumped system representation of a nutrient with an individual representation of algae. The IBM models are evaluated against a conventional PLM (because that is the traditional approach) and data from a number of steady and unsteady continuous (chemostat) and batch culture laboratory experiments. The stochastic IBM model fails the steady chemostat culture test, because it produces excessive numerical randomness. The deterministic cell cycle IBM model fails the batch culture test, because it has an abrupt drop in cell quota at division, which allows the cell quota to fall below the subsistence quota. The deterministic cell size IBM model reproduces the data and PLM results for all experiments and the model parameters (e.g. maximum specific growth rate, subsistence quota) are the same as those for the PLM. In addition, the model-predicted cell age, size (carbon) and volume distributions are consistent with those derived analytically and compare well to observations. The paper discusses and illustrates scenarios where intra-population variability in natural systems leads to differences between the IBM and PLM models.