The oxidation of cardiolipin by cytochrome c (cyt c) plays a crucial role in cyt c release from mitochondria at the initiation of apoptosis. Herein we report the first evidence of cytochrome c acting as a peroxygenase in the presence of cardiolipin-mimics. The interaction of cyt c and oleoyl-CoA in the presence of primary amines results in conformational change, hydrogen peroxide-mediated substrate oxidation, acyl transfer to form N-acyl fatty acid amides, increased peroxidase activity, and peroxygenase activity such as concerted epoxidation. We investigate the mechanism of earlier reports of acyl transfer activity, the role of cyt c, and how H2O2 is utilized. We observe and characterize a catalytic cycle wherein the Met80-Fe bond is first disrupted by the acyl tail of the oleoyl-CoA, the oleoyl-CoA thioester is then oxidized at sulfur by a peroxide-oxidized cyt c, the acyl tail is next transferred via nucleophilic substitution by a primary amine, and finally, an oxygen atom from H2O2 is transferred in a concerted fashion from the heme center to form an acyl tail epoxide. We employ several primary amines and acyl-CoAs to determine the scope and necessary tail length for this reaction. Our results suggest that cytochrome c can behave as both a peroxygenase and peroxidase, and that oleoyl-CoA may serve as an important cardiolipin-mimic for future structural studies.