Although it is now well established that in the Amazonian onchocerciasis focus, straddling between Venezuela and Brazil, the main vectors in the highland (hyperendemic) and lowland (hypoendemic) areas, are respectively Simulium guianense sensu lato Wise and S. oyapockense s.l. Floch and Abonnenc, investigation of the vectorial role of a third anthropophagic species, Simulium incrustatum Lutz has remained inconclusive. Here we compare the vector competence of S. incrustatum with that of S. oyapockense s.l. by conducting, in the Venezuelan part of the focus, a series of feeding experiments designed to analyze their relative: (a) microfilarial intakes when fed upon the same skin load; (b) proportions of microfilariae (mf) surviving damage inflicted by the cibarial armature (present in both species); and (c) infective (L3) larval outputs. Although the ability of S. oyapockense s.l. to ingest mf, for a given microfilaridermia, was markedly higher than that of S. incrustatum, the (density-dependent) proportions of those ingested mf that were damaged by the armature were also consistently higher, with the resulting output of L3 larvae being significantly lower in S. oyapockense s.l. than in S. incrustatum. These results indicate that S. incrustatum plays a more important role in onchocerciasis transmission in the Amazonian focus than previously realized. We discuss the implications of our findings for the control and elimination of onchocerciasis with mass administration of ivermectin in this focus, where the three main anthropophagic species often co-occur.