Whilst adaptation and phenotypic plasticity might buffer species against habitat degradation associated with global climate change, few studies making such claims also possess the necessary and sufficient data to support them. Doing so requires demonstration of heritable variation in traits affecting fitness under new environmental conditions. We address this issue using an emerging aquatic system to study adaptation to climate change, the crimson-spotted rainbowfish (Melanotaenia duboulayi), a freshwater species from a region of eastern Australia projected to be affected by marked temperature increases. Captive born M. duboulayi of known pedigree were used to assess the long-term effects of contemporary and 2070-projected summer temperatures on the expression of genes previously identified in a climate change transcriptomics (RNA-Seq) experiment. Nearly all genes responded to increasing temperature. Significant additive genetic variance explained a moderate proportion of transcriptional variation for all genes. Most genes also showed broad-sense genetic variation in transcriptional plasticity. Additionally, molecular pathways of candidate genes co-occur with genes inferred to be under climate-mediated selection in wild M. duboulayi populations. Together, these results indicate the presence of existing variation in important physiological traits, and the potential for adaptive responses to a changing thermal environment.