The relationship between cardiac energy metabolism and the depression of myocardial performance during oxygen deprivation has remained enigmatic. Here, we combine in vivo³¹P-NMR spectroscopy and MRI to provide the first temporal profile of in vivo cardiac energetics and cardiac performance of an anoxia-tolerant vertebrate, the freshwater turtle ( Trachemys scripta) during long-term anoxia exposure (∼3 h at 21°C and 11 days at 5°C). During anoxia, phosphocreatine (PCr), unbound levels of inorganic phosphate (effective P_i²⁻), intracellular pH (pH_i), and free energy of ATP hydrolysis (dG/dξ) exhibited asymptotic patterns of change, indicating that turtle myocardial high-energy phosphate metabolism and energetic state are reset to new, reduced steady states during long-term anoxia exposure. At 21°C, anoxia caused a reduction in pH_ifrom 7.40 to 7.01, a 69% decrease in PCr and a doubling of effective P_i²⁻. ATP content remained unchanged, but the free energy of ATP hydrolysis (dG/dξ) decreased from −59.6 to −52.5 kJ/mol. Even so, none of these cellular changes correlated with the anoxic depression of cardiac performance, suggesting that autonomic cardiac regulation may override putative cellular feedback mechanisms. In contrast, during anoxia at 5°C, when autonomic cardiac control is severely blunted, the decrease of pH_ifrom 7.66 to 7.12, 1.9-fold increase of effective P_i²⁻, and 6.4 kJ/mol decrease of dG/dξ from −53.8 to −47.4 kJ/mol were significantly correlated to the anoxic depression of cardiac performance. Our results provide the first evidence for a close, long-term coordination of functional cardiac changes with cellular energy status in a vertebrate, with a potential for autonomic control to override these immediate relationships.