The Deepwater Horizon disaster drew global attention to the toxicity of crude oil and the potential for adverse health effects among spill responders and numerous animal species in the northern Gulf of Mexico. Crude oil releases complex mixtures of polycyclic aromatic hydrocarbons (PAHs) into marine and terrestrial environments. In the 2010 spill, the oiled areas included pelagic spawning habitats for tunas, billfish, and other ecologically important top predators. During early ontogeny, the developing fish heart is more sensitive to PAH toxicity than any other organ. However, the precise PAHs that cause cardiotoxicity, as well as the mechanisms underlying contractile dysfunction, are not known. Here we use electrophysiological and confocal microscopy techniques in tunas and mackerels to demonstrate that phenanthrene, a PAH with a benzene 3-ring structure, is the key moiety altering cardiac excitation-contraction coupling. Mechanisms interfering with cardiac function include reduced Ca2+ transients and action potential prolongation due to hERG potassium channel blockade. In addition to petroleum based oil spills, there are many important environmental sources of phenanthrene, including urban air pollution. Our findings therefore suggest that phenanthrene may be a major worldwide cause of vertebrate cardiac arrhythmia.