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Epigenetic mechanisms govern cellular glucose sensing and GSIS by \u03b2 cells, but they remain incompletely defined. Here, we found that BAF60a functions as a chromatin regulator that sustains biphasic GSIS and preserves \u03b2 cell function under metabolic stress conditions. BAF60a was downregulated in \u03b2 cells from obese and diabetic mice, monkeys, and humans. \u03b2 cell\u2013specific inactivation of BAF60a in adult mice impaired GSIS, leading to hyperglycemia and glucose intolerance. Conversely, restoring BAF60a expression improved \u03b2 cell function and systemic glucose homeostasis. Mechanistically, BAF60a physically interacted with Nkx6.1 to selectively modulate chromatin accessibility and transcriptional activity of target genes critical for GSIS coupling in islet \u03b2 cells. A BAF60a V278M mutation associated with decreased \u03b2 cell GSIS function was identified in human donors. Mice carrying this mutation, which disrupted the interaction between BAF60a and Nkx6.1, displayed \u03b2 cell dysfunction and impaired glucose homeostasis. In addition, GLP-1R and GIPR expression was significantly reduced in BAF60a-deficient islets, attenuating the insulinotropic effect of GLP-1R agonists. 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