Despite much field and laboratory research, the origin of calcification in coccolithophores remains indeterminate. While most experiments on living species are not applicable to extinct taxa, long-term morphologic changes in lineages under well constrained oceanographic conditions may help elucidate the primary forcing on coccolithophore evolution if examined in the context of fundamental requirements (e.g., nutrient availability) of the living cell. The Order Discoasterales (66–1.92 Ma) was among the most prolific (>600 species, 16 genera) with greatest abundance and diversity in warm oligotrophic waters. Their coccoliths tell a story of morphologic changes that affected also their constituent elements resulting in lightweight constructions that became increasingly cavernous as oligotrophy increased in the Paleocene ocean, leading to increase in surface/volume ratio in keeping with increase in cell size. This likely constitutes direct evidence that coccoliths were involved in regulating cell physiology, both by maintaining a sufficient surface for nutrient absorption when cell volume increases or when nutrient content in seawater decreases, and by determining sinking rates. The cavernous nature of coccoliths further suggest mixotrophic physiology. Calcification may thus have been the innovation permitting the migration of the ancestral coccolithophore from nutrient-rich coastal waters to the blue ocean.