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The \u03b17 nicotinic acetylcholine receptor (\u03b17nAChR), which is a neurotransmitter receptor, exerts immunoregulatory effects. Recent advances have illuminated the evolution and functions of peripheral and cardiac B cells in heart disease. However, the role of \u03b17nAChR expressed by B cells in the progression of VMC has not been established. We revealed the neuroimmune communication landscape in the heart and found that the phenotypes of cardiac and splenic B cells and their \u03b17nAChR expression changed dynamically during the progression of VMC to dilated cardiomyopathy. \u03b17nAChR on B cells serves as a negative regulator by inhibiting their proinflammatory functions and signaling pathways. B cell\u2013specific \u03b17nAChR deficiency exacerbated myocardial inflammation, fibrosis, and cardiac dysfunction. However, these effects were abrogated in non-B cells from mice with IL-17A knockdown. Enhanced degradation of acetylcholine leads to an imbalance in cholinergic signaling, resulting in impaired neurotransmission. The acetylcholinesterase inhibitor pyridostigmine bromide could improve cardiac remodeling and prevent the progression of VMC to the chronic phase, which was partly dependent on the \u03b17nAChR on B cells. 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