Some species of termites evolved an outstanding reproductive strategy called asexual queen succession (AQS), in which the primary queen is replaced by multiple parthenogenetically produced daughters (neotenics) that mate with the primary king. When the primary king is eventually replaced, this time by sexually produced neotenic king(s), sex-asymmetric inbreeding occurs and the queen’s genome is more transmitted than that of the king, thereby increasing the reproductive value of female dispersers, and female-biased population sex ratio is expected. Yet, the life cycle, the breeding system dynamics and AQS modalities differ between AQS species, thereby modifying the relative genetic contribution of primary reproductives in the colony and thus also the equilibrium sex ratio. We estimated colonial and population sex ratio over two consecutive dispersal periods in a French Guiana population of Cavitermes tuberosus (Termitinae) in which the founding queen may be replaced only after colony maturity, some neotenic females may be sexually produced, and some female dispersers arise through parthenogenesis. Colonial sex ratio varied among colonies: primary-headed nests with higher within-nest relatedness produced more females than neotenic-headed nests with lower relatedness among individuals. Over the two dispersal periods, the population investment sex ratio fluctuated around 1:1, thereby confirming that AQS breeding system is not necessarily linked with female biased sex ratio. The balanced alate sex ratio, combined with the occurrence of sexually produced neotenic queens, is possibly the outcome of a queen-king conflict between the primary reproductives.