Summary Lifetime seed production can be constrained by shortfalls of pollen receipt (‘pollen limitation’). The ovule oversupply hypothesis states that, in response to unpredictable pollen availability, plants evolve to produce more ovules than they expect to be fertilized, and that this results in pollen limitation of seed production. Here, we present a cartoon model and a model of optimal plant reproductive allocations under stochastic pollen receipt to evaluate the hypothesis that an oversupply of ovules leads to increased pollen limitation. We show that an oversupply of ovules has two opposing influences on pollen limitation of whole‐plant seed production. First, ovule oversupply increases the likelihood that pollen receipt limits the number of ovules that can be fertilized (‘prezygotic pollen limitation’). Second, ovule oversupply increases the proportion of pollen grains received that are used to fertilize ovules (‘pollen use efficiency’). As a result of these opposing influences, ovule oversupply has only a modest effect on the degree to which lifetime seed production is constrained by pollen receipt, producing a small decrease in the incidence of pollen limitation. Ovule oversupply is not the cause of the pollen limitation problem, but rather is part of the evolutionary solution to that problem.