Cell division asymmetry underlies many fundamental biological processes, including the evolution of aging. Despite this importance, understanding whether the observed division asymmetry has been optimized by evolution remains little explored. Here we first show that size and transcription signal asymmetries have evolved to an optimum, as increased or decreased asymmetries lowers population growth. We then highlight how variance and covariance in growth and transcription signal asymmetry influence population growth. This latter exploration reveals how sensitive deviations to the optimum are, and that selective forces act primarily on variance in transcription signal asymmetry and less so on other cell intrinsic noise or growth asymmetries. Our findings are based on advancing integral projection models to two traits and we parameterize these models with single-cell data of mother and daughter E. coli bacterial cells collected using microfluidic devices. We discuss how trade-offs between growth and the transcription signal we explore has shaped this optimum. Our findings provide insights on how division asymmetries and resulting cellular heterogeneity can have profound biological consequences--contributing to processes such as cancer development, antibiotic treatment failure, and the rejuvenation of cell lineages, including in mammalian stem cells.