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. The electrogenic property of this pump, which originally evolved to balance intra- and extracellular osmotic pressures, seems a useful preadaptation for certain encoding paradigms, cell-intrinsic bursting dynamics, and accelerated ion homeostasis. We show that for nerve and muscle cells that need to be tonically active for long stretches of time (on the order of minutes to hours), the electrogenicy of the pump has further, less explored consequences that affect neuronal biophysical design as well as energy efficiency.To showcase this, we analyse the effects of Na+/K+-ATPase in a highly active excitable cell with a significant energetic demand: the weakly electric fish electrocyte. Electrocytes are entrained by a pacemaker, which transmits high firing rates that vary depending on social context. We show that tonic high frequency firing requires co-expression of Na+/K+-ATPase and 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. This suggests that even though Na+/K+-ATPase came as a useful preadaptation to generate action potentials in excitable cells, the fact that their original function required them to be electrogenic inevitably restricts excitable cell efficiency and design.