The evolution of the Na$^+$/K$^+$-ATPase in ancestral methanogenic archaea also lay the foundation for the energetics of energy-intensive signaling tissues like the metazoan nervous systems billions of years later [1]. The electrogenic property of this pump, which leads to activity-dependent feedback [2], seems a useful exaptation for certain encoding paradigms, cell-intrinsic bursting dynamics, and accelerated ion homeostasis [3-5]. For nerve and muscle cells that need to be tonically active for long stretches of time (on the order of minutes to hours), the electrogenicity of the pump has further, less explored consequences that may affect the biophysical markup of the membrane as well as energy efficiency. To demonstrate this, we analyse the effects of Na$^+$/K$^+$-ATPases in a highly active excitable cell with a significant energetic demand: the weakly electric fish electrocyte [6]. Electrocytes are entrained by a pacemaker, which fires at high rates that vary depending on social context. We show that consistent rapid firing requires co-expression of Na$^+$/K$^+$-ATPases and ion channels that facilitate a constant inward current such as sodium leak channels, which reduces action potential efficiency. We furthermore show that behaviorally relevant deviations from baseline firing induce significant alterations in intrinsic electrocyte properties through pump rate adaptation. To ensure reliable entrainment of the electrocyte by the pacemaker despite these cell-intrinsic variations, sufficient synaptic coupling and extracellular potassium buffering are required. Lastly, we postulate that a strong voltage-dependence of the Na$^+$/K$^+$-ATPase can attenuate aforementioned effects and reduces the requirement for regulatory mechanisms. This suggests that even though Na$^+$/K$^+$-ATPases came as a useful exaptation to generate action potentials in excitable cells, the fact that their original function required them to be electrogenic inevitably constrains the ion channel markup and restricts the excitable cells’ efficiency.