P1a and P1b are two serine proteases of Cucumber vein yellowing virus (an ipomovirus). They belong to the group of P1 factors present at the N terminus of the polyproteins of most members of the family Potyviridae. The present work compares the protease activities of P1a and P1b in different experimental systems. The findings made regarding how these two proteases work, such as the requirement for a host factor by P1a but not by P1b, underscore important differences in their catalytic activity that point towards their undergoing divergent evolution involving the acquisition of mechanistic variations. The expression of several truncated forms of P1b in bacteria and in planta helped define the protease domain of P1b, along with other important features such as its apparently in cis mode of action. Recent phylogenetic data, together with the present results, allow an appealing hypothesis to be proposed regarding P1 evolution and its involvement in potyvirid speciation.