γδ T cells are guardians at barrier sites and rapidly respond to the presence of extracellular fungi, bacterial infections, and cellular stress by producing chemokines and cytokines. However, little is known about their steady state role in non-barrier tissues. Here, we characterize a highly enriched, tissue-resident population of γδ T cells in adipose tissue that regulates age-dependent adipose Treg expansion and controls core body temperature in response to environmental fluctuations. These adipose γδ T cells express and rely on the transcription factor PLZF and transcriptional profiling of PLZF⁺ γδ T cells reveals their innate-phenotype and functional capacity to produce TNF and IL-17A. Mechanistically, TNF and IL-17A synergize to enhance IL-33 production by adipose stromal cells and augment Treg numbers. As such, mice genetically deficient in PLZF⁺ γδ T cells or IL-17A in vivo, exhibit striking reductions in both ST2⁺ Tregs and IL-33 levels in visceral adipose tissue. Surprisingly, we find that mice deficient in PLZF⁺ γδ T cells also lack the ability to regulate core body temperature at thermoneutrality and cold challenge due to their inability to support UCP-1 dependent adaptive thermogenesis. γδ T cell regulation of body temperature thus opens a new dimension in adipose biology, whereby the dynamic cross talk between innate lymphocytes and tissue-specific stromal cells dictates local immune homeostasis and systemic energy expenditure. Together, our studies underscore the emerging roles of innate γδ T cells as critical modulators of both immune and tissue homeostatic biology.