Electrogenic Na⁺/K⁺ ATPases (NKAs) control β-cell Ca²⁺ influx and insulin secretion by integrating the signal strength of stimulatory G protein (G_s)-coupled ligands (e.g., GLP-1, glucagon) and inhibitory G protein (G_i)-coupled ligands (e.g., somatostatin, epinephrine). However, there is a significant gap in our understanding of how specific NKA subunits contribute to β-cell function. Here, we demonstrate that the NKA β1-subunit (NKAβ1) is highly expressed and functional at the plasma membrane of mouse and human β-cells. β-cell-specific NKAβ1 knockout improves glucose tolerance and hepatic insulin sensitivity, coinciding with enhanced first- and second-phase glucose-stimulated insulin secretion (GSIS). Electrophysiological studies reveal that β-cell NKAβ1 enhances somatostatin-induced NKA currents, increases action potential afterhyperpolarization amplitude, and accelerates action potential frequency. Loss of NKAβ1 delays glucose-stimulated Ca²⁺ entry by impairing glycolysis-dependent NKA activation and reduces Na⁺ clearance efficiency during Ca²⁺ oscillations, resulting in prolonged silent phases. Thus, glycolytic stimulation of Na⁺ influx dictates silent phase duration via the kinetics of Na⁺ clearance by NKA, which is diminished in β-cells without NKAβ1. Furthermore, NKAβ1 differentially modulates β-cell G protein-coupled receptor (GPCR) signaling by attenuating G_i-GPCR effects and augmenting G_s-coupled GLP-1 receptor-mediated cAMP production and Ca²⁺ entry. β-cell NKAβ1 knockdown in human pseudoislets led to tonically elevated intracellular Ca²⁺ and increased insulin secretion. These findings establish NKAβ1-containing NKA complexes as critical regulators of β-cell electrical activity, Ca²⁺ oscillations, and secretory patterns, with direct consequences for systemic glucose homeostasis.