Androgen vasorelaxing action is a subject of recent interest. We investigated the involvement of L-type voltage-operated Ca²⁺ channels (L-VOCCs), K⁺ channels, intracellular Ca²⁺ concentration ([Ca²⁺]i) and cAMP in the vasorelaxing effect of testosterone and 5-dihydrotestosterone (5-DHT) on rat thoracic aorta. Isolated aortic rings were used to study the vasorelaxing potency of testosterone and 5-DHT on KCl- and noradrenaline-induced contractions. Patch-clamp was used to analyze androgen effects on Ca²⁺ inward and K⁺ outward currents. The fluorescence technique was used to evaluate [Ca²⁺]i in single myocytes; moreover, simultaneous measurements of [Ca²⁺]i and vascular contraction were evaluated. 5-DHT was more potent than testosterone to relax KCl-induced contraction but they were equipotent to relax noradrenaline contraction. L-type Ca²⁺ currents were blocked by nifedipine, both androgens and an estrogen in a concentration-dependent manner and the order of potency was: testosterone>nifedipine>5-DHT>17-estradiol. We observed that testosterone has different mechanism of action by the concentration range used: at nM concentrations it was a powerful L-VOCCs antagonist, while at µM concentrations it was observed that: (i) its Ca²⁺ antagonist property is reverted by increasing the L-type inward Ca²⁺ currents (Ca²⁺ agonist property); and (ii) the [Ca²⁺]i and cAMP production were increased. The total K⁺ currents were unaffected by testosterone or 5-DHT. The data show that 5-DHT-induced vasorelaxation is due to its selective blockade on L-VOCCs (from nM to µM concentrations) but testosterone-induced vasorelaxation involves concentration-dependent additional mechanisms: acting as an L-VOCCs antagonist at low concentrations, and increasing [Ca²⁺]i and cAMP production at high concentrations.