Significance Populations of larger organisms should be more efficient in their resource use, but grow more slowly, than populations of smaller organisms. The relations between size, metabolism, and demography form the bedrock of metabolic theory, but most empirical tests have been correlative and indirect. Experimental lineages of Escherichia coli that evolved to make larger cells provide a unique opportunity to test how size, metabolism, and demography covary. Despite the larger cells having a relatively slower metabolism, they grow faster than smaller cells. They achieve this growth rate advantage by reducing the relative costs of producing their larger cells. That evolution can decouple the costs of production from size challenges a fundamental assumption about the connections between physiology and ecology.