Primitive life must have possessed the essential features of modern cellular life, but without highly evolved proteins to perform dynamic functions such as nutrient transport and membrane remodeling. Here, we consider the membrane properties of protocells — minimal cells with hereditary material, capable of growth and division — and how these properties place restrictions on the components of the membrane. For example, the lipids of modern membranes are diacyl amphiphilic molecules containing well-over 20 carbons in total. Without proteins, these membranes are very stable and kinetically trapped. This inertness, combined with the need for enzymes to synthesize them, makes modern diacyl amphiphiles unsuitable candidates for the earliest membranes on Earth. We, therefore, discuss the progress made thus far with single-chained amphiphiles, including fatty acids and mixtures of fatty acids with related molecules, and the membrane-related research that must be undertaken to gain more insight into the origins of cellular life.