Mitochondria are essential for complex multicellular life, suppling ~90% of cellular power as ATP. In fish, mitochondria fail (mtTcrit) just below the upper temperature tolerance limit, leading to heart failure and death. However, the mechanisms that induce mitochondrial disruption remain unclear. The traditional view of how elevated temperatures impact mitochondrial function assumes mitochondrial membrane potential (mtMP) is uniformly distributed across the inner mitochondrial membrane (IMM), and becomes permeable to ion leak with temperature. This collapses the mtMP, the driving force of ATP synthesis. Recently, nanoscale mitochondrial imaging revealed that each crista generates an independent mtMP, suggesting the IMM structures are essential for mitochondrial function. We hypothesized that acute thermal-stress alters mitochondrial ultrastructure, contributing to heart failure at elevated temperatures. We assessed mitochondrial respiration and swelling concurrently in two wrasse species from different thermal-environments: cold-temperate N.fucicola and tropical C.sordidus. We also investigated changes in mitochondrial density and cristae structure in cardiac tissue following incubation at temperatures spanning and exceeding each species’ natural habitat temperature. At ~mtTcrit, cristae lost structural integrity, inter-cristae distance increased, and mitochondria swelled. This suggests that loss of mitochondrial ultrastructure underlies cardiac mitochondrial failure with acute warming, and may limit the thermal habitat range of species.