Many traits studied in ecology and evolutionary biology change their expression in response to a continuously varying environmental factor. One well-studied example are thermal performance curves (TPCs); continuous reaction norms that describe the relationship between organismal performance and temperature and are useful for understanding the trade-offs involved in thermal adaptation. We assayed TPCs for locomotor activity in a set of 66 spontaneous mutation accumulation lines in the fly Drosophila serrata. Factor-analytic modeling of the mutational variance-covariance matrix, M, revealed support for three axes of mutational variation in males and two in females. These independent axes of mutational variance corresponded well to the major axes of TPC variation required for different types of thermal adaptation; ‘faster-slower’ representing changes in performance largely independent of temperature, and the ‘hotter-colder’ and ‘generalist-specialist’ axes, representing trade-offs. In contrast to its near-absence from standing variance in this species, a ‘faster-slower’ axis, accounted for most mutational variance (75% in males and 66% in females) suggesting selection may easily fix or remove these types of mutations in outbred populations. Axes resembling the ‘hotter-colder’ and ‘generalist-specialist’ modes of variation contributed less mutational variance but nonetheless point to an appreciable input of new mutations that may contribute to thermal adaptation.