Bdellovibrio bacteriovorus is an obligate predatory bacterium that exclusively feeds upon other bacteria after invading their periplasm. Within the prey, B. bacteriovorus elongates and produces variable numbers of progeny through non-binary division. By monitoring chromosome dynamics, cell growth, and cell division in single predator cells, we found that prey cell size and nutritional content have distinct impacts on the predator’s cell cycle progression. Our results indicate that B. bacteriovorus finely adjusts its growth phase to the variability of its prey, optimizing the use of available resources, while also featuring robust temporal coordination of cell cycle processes. In contrast to this endobiotic predation mode, epibiotic predators such as the closely related Bdellovibrio exovorus, remain attached to the prey cell surface while growing and dividing. We provide the first live-cell imaging of this predation mode, revealing a novel cell division pattern and challenging a previously proposed defence mechanism against predators. Altogether, our data imply that endo- and epibiotic feeding strategies differently shape the cell cycle of bacterial predators.