This essay considers the ontogeny and phylogeny of the cranial neural circuitry producing rhythmic behaviors in vertebrates. These behaviors are characterized by predictable temporal patterns established by a neuronal network variously referred to as either a pacemaker, neural oscillator or central pattern generator. Comparative vertebrate studies have demonstrated that the embryonic hindbrain is divided into segmented compartments called rhombomeres, each of which gives rise to a distinct complement of cranial motoneurons and, as yet, unidentified populations of interneurons. We now propose that novel rhythmic circuits were innovations associated with the adoption of cardiac and respiratory pumps during the protochordate-vertebrate transition. We further suggest that the pattern-generating circuits of more recent innovations, such as the vocal, electromotor and extraocular systems, have originated from the same Hox gene-specified compartments of the embryonic hindbrain (rhombomeres 7–8) that gave rise to rhythmically active cardiac and respiratory circuits. Lastly, we propose that the capability for pattern generation by neurons originating from rhombomeres 7 and 8 is due to their electroresponsive properties producing pacemaker oscillations, as best typified by the inferior olive which also has origins from these same hindbrain compartments and has been suggested to establish rhythmic oscillations coupled to sensorimotor function throughout the neuraxis of vertebrate