Field and laboratory findings implicated Culex pipiens as a vector of Rift Valley fever (RVF) virus during the 1977–1978 epizootics/epidemics in Egypt. This study evaluated changes in infection and transmission rates, and viral titers in F1 through F16 generation Cx. pipiens mosquitoes orally infected with RVF virus. Infection and transmission rates of RVF virus by this species changed significantly during the colonization process. However, the ultimate viral titers of either the transmitting or the infected nontransmitting mosquitoes were not affected by the colonization process. Following ingestion of virus, Cx. pipiens could be separated into three distinct subpopulations, an uninfected group and two types of infected mosquitoes—transmitters and nontransmitters. Transmitters contained significantly more virus (approximately 100-fold) than nontransmitters. These results demonstrated that not every infected female mosquito should be considered a competent vector, even if the species (population) is known to be a primary vector. Transmission was also accomplished by probing mosquitoes which were unsuccessful in obtaining a blood meal. These data document the long-held suspicion that vector competence studies based upon laboratory-colonized specimens may not represent the field situation.