Thermal adaptation may be key for species persistence in the face of ongoing climate change. Thermal adaptation can be achieved via phenotypic plasticity or rapid evolution of genetically fixed traits. Metabolism dictates energetic demands of organisms, linking fitness with environmental resources and defining organisms ecological role. Metabolic theory of ecology (MTE) proposes universal allometric scaling rules for metabolic rate with body size and temperature; therefore, it is used to parametrized models to predict ecological outcomes of climate change, neglecting intraspecific variability and potential for thermal adaptation of metabolic traits. To investigate thermal adaptation of metabolism and the underlying mechanisms behind it, we perform a common garden experiment, using invasive mosquitofish from six recently colonized (<100 years) geothermal ponds, spanning a wide temperature gradient (18°C-33°C). Mosquitofish from these geothermal systems show differences in the allometry and temperature dependence of metabolism in nature, but is not clear if differences are due to phenotypic plasticity or genetic change. We common reared F0 and F1 fish at 26°C, and subsequently, we measured metabolic and excretion rates from F2 fish at four rearing temperatures: 23°C, 26°C, 30° and 32°C. The allometry and temperature sensitivity of metabolism and excretion differed from MTE predictions when individuals were analysed by origin and rearing temperatures. The differences in these parameters do not follow a clear linear pattern when comparing across rearing temperature and origin temperature gradients. F2 fish reared at 26°C show the most differences in metabolic trait suggesting that mosquitofish metabolism is extremely plastic to temperature. Our results suggest that intraspecific variation in thermal history does not have simple effects on metabolic rate, making the assumptions of MTE inadequate for predictions at the population level, where complex processes may be shaping organism energetic demands.