Extensive visceral adipose tissue (VAT) accumulation increases the risk of developing metabolic and cardiovascular diseases. The ability of adipose tissue to combust energy through non-shivering thermogenesis is viewed as a beneficial mechanism to counteract these severe metabolic issues. Yet, efforts to activate a thermogenic program in VAT remain elusive and limited to transgenic interventions or drastic temperature alterations. Here, we report extensive activation of VAT thermogenesis by exposing microbiota-depleted mice to cold. These mice exhibited a drastic reduction in visceral and overall adiposity, accompanied by improved respiration capacity and insulin sensitivity. The VAT displayed a multilocular morphology with a thermogenic program that was independent of UCP1 and alternatively differentiated macrophages. Combining adipocyte lineage tracing with snRNA-seq and spatial transcriptomics revealed a subset of adipocytes originating from existing mature adipocytes, which use a distinct, noncanonical thermogenesis process based on futile cycles. The functional remodeling of the VAT is driven by an increased sympathetic tonus, evidenced by increased systemic and local norepinephrine (NE) levels, along with the denser sympathetic nerve network in the VAT. Mechanistically, VAT of Cax mice shows consistent upregulation of Elovl3, a gene involved in the production and degradation of long and very long chain fatty acids. Tissue-restricted pgVAT Elovl3 deletion led to an increase in pgVAT mass during Cax treatment, coupled to a decrease in some of the common browning markers. Systemic depletion of Ucp-1-expressing cells in brown and subcutaneous adipose tissue (BAT and SAT, respectively) during cold led to a profound increase in VAT browning, indicating that VAT acts as a third line of defense that ensures thermogenic homeostasis. These findings reveal previously underexplored aspects of VAT and uncover a unique plasticity of this type of fat, opening a window for new therapeutic solutions in preventing and treating obesity.