Little is known about the mechanisms underpinning thermal plasticity of vertebrate hearts. Bluefin tuna hearts offer a unique model to investigate processes underlying thermal acclimation. Their hearts, while supporting an endothermic physiology, operate at ambient temperature and are presented with a thermal challenge when migrating to different thermal regimes. Here, we examined the molecular responses in atrial and ventricular tissues of pacific bluefin tuna acclimated to 14^oC, 20^oC and 25^oC. qPCR studies showed an increase in sarcoplasmic reticulum Ca²⁺ATPase gene expression with cold acclimation and an induction of Na⁺/Ca²⁺-exchanger gene at both cold and warm temperatures. This data provide evidence for thermal plasticity of excitation-contraction coupling gene expression in bluefin tunas and indicate an increased capacity for internal Ca²⁺ storage in cardiac myocytes at 14^oC. Transcriptomic analysis showed profound changes in cardiac tissues with acclimation. A principal component analysis revealed that temperature effect was greatest on gene expression in warm-acclimated atrium. Overall data showed an increase in cardiac energy metabolism at 14^oC, potentially compensating for cold temperature to optimize bluefin tuna performance in colder oceans. In contrast, metabolic enzyme activity and gene expression data suggest a decrease in ATP production at 25^oC. Expression of genes involved in protein turnover and molecular chaperons was also decreased at 25^oC. Expression of genes involved in oxidative stress response and programmed cell-death suggest an increase in oxidative damage and apoptosis at 25^oC, particularly in the atrium. These findings provide insights into molecular processes that may characterize cardiac phenotypes at upper thermal limits of teleosts.