Differences in the dispersal flight patterns among termite families are correlated with the difference between the two life history characteristics exhibited by this group: “separate-piece nesters” versus “single-piece nesters.” However, information remains limited on the phenology and the life history characteristics of single-piece nesters, impeding our understanding of this topic. We report the flight phenology of an Asian single-piece nester termite Neotermes koshunensis on Okinawa Island, Japan. In 1983–1984, a light-trap survey showed that N. koshunensis exhibited an extended dispersal flight period from late April to early November, peaking in June, with a female-biased sex ratio. Between 1983 and 2012, the collection of 134 whole colonies of N. koshunensis from the surrounding area confirmed the presence of alates and pre-alate nymphs within the colonies over 7 months, reflecting the extended flight season of this termite species, probably in association with the extended dispersal flight season. However, in some cases, alates and pre-alate nymphs were also retained in the colonies after the dispersal flight season (i.e., winter, from December to February). The daily number of trapped alates in 1983 was positively correlated with temperature and relative humidity; however, alate production inside the colony was also positively correlated with temperature, relative humidity, and precipitation. Thus, these environmental factors might promote the flight activity of this termite by enhancing alate production inside the colony. Furthermore, temperature also had a significantly positive effect in the model incorporating the density of alates in the colony, along with environmental factors; thus, temperature might facilitate the release of alate from colonies. The accumulation of information on the phenology and life history characteristics of alate advances our understanding of the different dispersal strategies used by termites, providing insights into how the different families have evolved.