To test their virus susceptibility and capacity as transmission vectors, Japanese Culicoides species were artificially fed a mixture of Akabane virus (AKAV) and bovine blood, and virus recovery was attempted from infected midges 9–11 d post-exposure. Culicoides tainanus, C. punctatus, C. humeralis, C. jacobsoni, C. oxystoma, and C. asiana were found to be orally susceptible to AKAV. Virus titers in single infected midges of C. tainanus, C. oxystoma, C. punctatus, and C. jacobsoni ranged from 10^0.75 to 10^4.0 TCID₅₀ (tissue culture infectious dose). The titers in the infected C. oxystoma were significantly higher than those in the other infected species. Viral RNA was detected from both midges testing positive and those testing negative for infectious virus particles, but the viral RNA copies in the infectious virus-negative midges were significantly lower than those in the infectious virus-positive midges. Lower viral amplification, limited dissemination or both caused by tissue barriers might occur in infected midges from which infectious viruses were undetectable. A fully disseminated infection was developed in orally infected C. oxystoma and C. tainanus. This finding indicates their capacity to transmit AKAV, assuming that salivary gland barriers have limited effects on viral entry to and replication in salivary gland tissue. This result also suggests that the other orally susceptible species are potentially competent for AKAV transmission and would be considered active vectors of its spread.