The walls of the mammalian aorta and pulmonary artery are characterized by diverging morphologies and mechanical properties, which have been correlated with high systemic and low pulmonary blood pressure, as a result of intraventricular pressure separation. However, the relationship between intraventricular pressure separation and diverging aortic and pulmonary artery wall morphologies and mechanical characteristics is not understood. The snake cardiovascular system poses a unique model for the study of this relationship, as representatives both with and without intraventricular pressure separation exist. In this study, we performed uniaxial tensile testing on vessel samples taken from the aortas and pulmonary arteries of the Madagascar ground boa, Acrantophis madagascariensis, a species without intraventricular pressure separation. We then compared these morphological and mechanical characteristics with samples from the ball python, Python regius, and the yellow anaconda, Eunectes notaeus – species with and without intraventricular pressure separation, respectively. Our data suggest that although the aortas and pulmonary arteries of A. madagascariensis respond similarly to the same intramural blood pressure, they diverge in morphology, and that this attribute extends to E. notaeus. In contrast, P. regius aortas and pulmonary arteries diverge both morphologically and in terms of their mechanical properties. Our data indicate that intraventricular pressure separation cannot fully explain diverging aortic and pulmonary artery morphologies. Following the law of Laplace, we propose that pulmonary arteries of small luminal diameter represent a mechanism to protect the fragile pulmonary vasculature by reducing the blood volume that passes through, to which genetic factors may contribute more strongly than physiological parameters.