Adipose tissue macrophages (ATMs) can promote beige adipose thermogenesis by altering local sympathetic activity. This study demonstrates that ATMs have a direct beige-promoting function independent of the sympathetic system. The transcription factor Ets1 in adipocytes is identified as a key mediator in this process. M2 macrophages suppress Ets1 expression in adipocytes, activate mitochondrial biogenesis, and inhibit mitochondrial clearance, thereby increasing mitochondrial numbers and promoting beige adipogenesis. Male adipocyte Ets1 knock-in mice are cold intolerant, while male mice lacking Ets1 in adipocytes show enhanced energy expenditure and resistance to metabolic disorders caused by a high-fat diet. These findings elucidate a direct communication between M2 macrophages and adipocytes and uncover the role of Ets1 in responding to macrophage signals and negatively governing mitochondrial content and beige adipocyte formation.Adipose tissue macrophages (ATMs) can promote beige adipose thermogenesis by altering local sympathetic activity. This study demonstrates that ATMs have a direct beige-promoting function independent of the sympathetic system. The transcription factor Ets1 in adipocytes is identified as a key mediator in this process. M2 macrophages suppress Ets1 expression in adipocytes, activate mitochondrial biogenesis, and inhibit mitochondrial clearance, thereby increasing mitochondrial numbers and promoting beige adipogenesis. Male adipocyte Ets1 knock-in mice are cold intolerant, while male mice lacking Ets1 in adipocytes show enhanced energy expenditure and resistance to metabolic disorders caused by a high-fat diet. These findings elucidate a direct communication between M2 macrophages and adipocytes and uncover the role of Ets1 in responding to macrophage signals and negatively governing mitochondrial content and beige adipocyte formation.