The typical fish heart has a spongy trabeculated ventricular myocardium (spongiosa) supplied by the venous blood of the intertrabecular spaces (lacunae); hence it is called a “venous heart.” However, in some fishes a more complex ventricular muscle is found (mixed type), in which the spongiosa is covered by an outer layer of densely arranged myocardial bundles (compacta). The compacta receives oxygenated blood from the coronary vessels. The objective of this study was to investigate relations between myoarchitecture and blood supply with an emphasis on the hitherto unexplored, putative vascular connections between the arterial and the lacunary circuits. Using histological methods combined with vascular cast techniques and India ink injections, it was possible to define four different types of ventricular myocardium and its microvsculature. In some of them an intramural network arises from the subepicardial arterial system supplying the compacta and also is distributed to the spongiosa. Extensive arterio-luminal vessels connect this coronary bed with the lacunary circuit of the spongiosa, so realizing the first evolutionary step of the Thebesian system. The highest development of these connections is found in some very active pelagic fishes. The functional morphology of these vascuar patterns is discussed in relation to the phylogenetic and functional context of the fish heart. It appears that the concept of the piscine heart as a typical “venous” type is an oversimplified generalization, at least on morphological grounds.