This essay addresses the fundamental mechanism underlying the precise regulation of PaCO2 during steady states of air-breathing eupnea and hyperpnea. First, an argument is made for CO₂/H⁺ chemoreception as an important compensatory feedback regulator of breathing and breathing stability, especially during nonrapid eye movement (NREM) sleep. Tonic contributions to respiratory drive occur from the carotid chemoreceptors and retrotrapezoid nucleus (RTN). A case against chemoreception of Pco₂ as the primary homeostatic PaCO2 regulator is made based on conditions where precise PaCO2 control during air-breathing exists even when ventilatory responsiveness to raised Pco₂ is markedly subnormal or when a measurable PaCO2 error signal is nonexistent. Alternatively, a case is made that homeostatic ventilatory control incorporates information critically dependent on pulmonary CO₂ exchange, as revealed when: 1) V̇co₂, per se, is altered at rest or exercise; 2) V_d/V_T is raised or lowered; and 3) the resting PaCO2 set point is changed, thereby changing respiratory system plant gains. In each of these common conditions, substantial ventilatory adjustments occur to achieve near-proportional V̇a:V̇co₂ linkages at rest and/or exercise with no coincidence changes in CO₂ chemoreception. We view this V̇co₂-mediated mechanism as a dedicated tracking system for alveolar ventilation that provides an essential underpinning in a traditional hybrid model of homeostatic ventilatory control. Although some potential mediators of these V̇co₂ effects have been suggested, such as an integrative role for the RTN, they remain inadequately explored. It is time to restart enquiry, using modern neuroscience approaches, into the mediation of V̇co₂ as the critical underpinning to PaCO2 homeostasis.