Blubber, the lipid-rich hypodermis of cetaceans, functions in thermoregulation, buoyancy control, streamlining, metabolic energy storage, and locomotion. This study investigated the development of this specialized hypodermis in bottlenose dolphins (Tursiops truncatus) across an ontogenetic series, including fetuses, neonates, juveniles, subadults, and adults. Blubber samples were collected at the level of the mid-thorax, from robust specimens (n = 25) that stranded along the coasts of North Carolina and Virginia. Blubber was dissected from the carcass and its mass, and the depth and lipid content at the sample site, were measured. Samples were prepared using standard histological methods, viewed by light microscopy, and digital images of blubber captured. Images were analyzed through the depth of the blubber for morphological and structural features including adipocyte size, shape, and numbers, and extracellular, structural fiber densities. From fetus to adult, blubber mass and depth increased proportionally with body mass and length. Blubber lipid content increased dramatically with increasing fetal length. Adult and juvenile blubber had significantly higher blubber lipid content than fetuses, and this increase was reflected in mean adipocyte size, which increased significantly across all robust life history categories. In juvenile, subadult, and adult dolphins, this increase in cell size was not uniform across the depth of the blubber, with the largest increases observed in the middle and deep blubber regions. Through-depth counts of adipocytes were similar in all life history categories. These results suggest that blubber depth is increased during postnatal growth by increasing cell size rather than cell number. In emaciated adults (n = 2), lipid mobilization, as evidenced by a decrease in adipocyte size, was localized to the middle and deep blubber region. Thus, in terms of both lipid accumulation and depletion, the middle and deep blubber appear to be the most metabolically dynamic. The superficial blubber likely serves a structural role important in streamlining the animal. This study demonstrates that blubber is not a homogeneous tissue through its depth, and that it displays life history-dependent changes in its morphology and lipid content.