A key adaptation of mammals to their environment is their ability to maintain a constant high body temperature, even at rest, under a wide range of ambient temperatures. In cold climates, this is achieved by an adaptive production of endogenous heat, known as nonshivering thermogenesis (NST), in the brown adipose tissue (BAT). This organ, unique to mammals, contains a very high density of mitochondria, and BAT correct functioning relies on the correct functioning of its mitochondria. Mitochondria enclose proteins encoded both in the maternally inherited mitochondrial genome and in the biparentally inherited nuclear genome, and one overlooked hypothesis is that both genomes and their interaction may shape NST. By housing under standardised conditions wild-derived common voles (Microtus arvalis) from two distinct evolutionary lineages (Western and Central), we show that Western voles had greater NST than Central voles. By introgressing those two lineages over at least 9 generations, we then experimentally tested the influence of the nuclear and mitochondrial genomes on NST and related phenotypic traits. We found that between-lineage variation in NST and BAT size were significantly influenced by the mitochondrial and nuclear genomes, respectively, with the Western mitochondrial genotype being associated with higher NST and the Western nuclear genotype with a larger BAT. There were significant mito-nuclear interactions on whole animal body weight and resting metabolic rate. Hybrid voles were lighter and had higher resting metabolic rate. Overall, our findings turn new light on the influence of the mitochondrial and nuclear genomes on thermogenesis and building adaptation to the environment in mammals.