Circulation of the blood is a fundamental physiological function traditionally ascribed to the pressure‐generating function of the heart. However, over the past century the ‘cardiocentric’ view has been challenged by August Krogh, Ernst Starling, Arthur Guyton and others, based on haemodynamic data obtained from isolated heart preparations and organ perfusion. Their research brought forth experimental evidence and phenomenological observations supporting the concept that cardiac output occurs primarily in response to the metabolic demands of the tissues. The basic tenets of Guyton's venous return model are presented and juxtaposed with their critiques. Developmental biology of the cardiovascular system shows that the blood circulates before the heart has achieved functional integrity and that its movement is intricately connected with the metabolic demands of the tissues. Long discovered, but as yet overlooked, negative interstitial pressure may play a role in assisting the flow returning to the heart. Based on these phenomena, an alternative circulation model has been proposed in which the heart functions like a hydraulic ram and maintains a dynamic equilibrium between the arterial (centrifugal) and venous (centripetal) forces which define the blood's circular movement. In this focused review we introduce some of the salient arguments in support of the proposed circulation model. Finally, we present evidence that exercising muscle blood flow is subject to local metabolic control which upholds optimal perfusion in the face of a substantive rise in muscle vascular conductance, thus lending further support to the permissive role of the heart in the overall control of blood circulation.