Perhaps the defining feature of the eukaryotic cell is its organization into membrane-bound compartments known as organelles. While the processes underlying the biogenesis of individual organelles are often well-known the precision with which individual cells exert quantitative control over individual organelle properties, such as number and size, and coordinate these properties at systems-scale across the cell’s many different types of organelles remain frontier problems in cell biology and biophysics. Using a combination of theory and quantitative experiment, I will. describe out recent efforts to show that cells exhibit substantial limits both the precision with which they can control organelle numbers and sizes, but despite this appear to collectively organize organelle biogenesis into specific “modes” when faced with the need to respond to environmental and genetic perturbations.