Cytoplasmic dynein is a molecular motor that transports a multitude of cargos towards the microtubule (MT) minus-end inside cells. The mechanism of dynein motility remained unclear, due to its large size and the complexity of its structure. Using high precision single molecule imaging approaches, we observed that dynein motility is a result of complex structural changes driven by ATP hydrolysis and the mechanism is fundamentally distinct from that of kinesin and myosin motors. The two motor domains (heads) of dynein move independently along the MT. Processivity minimally requires only one active head, provided that its linker is tethered to a MT. The heads experience intramolecular tension through their linker regions when they are separated away from each other. Tension on the linker inhibits ATP-dependent release partially coordinates the motility of the heads. The minus-end directionality is determined by the asymmetric binding and release properties of the MT binding interface. On the basis of these measurements, we developed a quantitative model that describes the basis of dynein processivity, directionality and force generation.