Brown adipose tissue (BAT) is involved in dissipating energy as heat (non-shivering thermogenesis), not only under cold exposure but also in the dissipation of excess ingested energy. Therefore, harnessing energy utilisation by BAT is a potential avenue to combat weight gain and its comorbidities. Dietary macronutrient composition can directly influence BAT size and has recently been shown to influence BAT size of daughters through non-genetic effects in the patriline of C57BL/6J mice. However, the effects of dietary macronutrient composition and any non-genetic paternal effects on BAT function have yet to be characterised. Using the Geometric Framework for Nutrition, we investigated the effects of dietary protein, carbohydrate, and fat composition on the BAT proteome in male mice (F0) and intergenerational effects in their offspring (F1). In F0 males, >50% of the proteome was affected by dietary macronutrient composition, with distinct clusters of proteins that responded to diet in similar ways. We identified two clusters with inverse expression patterns that correlated with BAT weight. Notably, Ucp1 was reduced on low fat diet compositions that promoted increased BAT mass, while on those same diets there were increased levels of proteins involved in protein turnover. These diets also led to a reduction in proteins involved in purine biosynthesis (often Ucp1 inhibitors) and increased Hsl, which facilitates free fatty acid release, critical for Ucp1 activation. We did not find any effects of paternal diet on the BAT proteome in sons, but paternal protein intake negatively affected Basigin expression in daughters; a protein that regulates Ucp1 transcription. Our study is the first characterisation of BAT protein abundance across a broad range of dietary macronutrient compositions and across two generations, with implications for our understanding of non-shivering thermogenesis and metabolism.