Conflicts over reproduction are common in animal societies and they are especially pronounced in groups of totipotent individuals. Workers in the drywood termite Cryptotermes secundus are totipotent. They can gain direct fitness via dispersal as winged sexual or inheritance of the natal nest as neotenic replacement reproductive. In this study we examined the actual conflict behaviour in C. secundus, possible mechanism of conflict-regulation, and factors influencing the conflict intensity. Cuticular hydrocarbons provided the information about nestmates which is required for mechanisms of conflict-resolution to work: they were (i) caste-specific, (ii) honest signal of fertility in neotenic queens, as they are reflecting the underlying JH titres mediated via caste-specific Neofem4 expression, and (iii) may also be informative enough to allow kin discrimination. Kin discrimination in C. secundus depended on social context and the individuals’ developmental potential. Sterile soldiers for example showed nepotistic grooming independent from the social context, but affected by wood resource, in contrast to workers that did not react to varying relatedness. Individuals showed distinct behavioural profiles before and during conflict, reflecting their reproductive potential: most prominent in the distinction were the dominance behaviour butting and proctodeal trophallaxis. The proposed role of trophallaxis as honest signal and inhibitory means in regulating reproductive development in C. secundus could be confirmed. Conflict intensity was greatly influenced by wood resource: workers were more likely to stay and fight for inheritance within nests that are resource rich, while when food gets limited dispersal conflict was most pronounced. Thus, individuals did continually assess the ecological (resources) and societal conditions (presence of reproductives, relatedness) and adjusted their developmental decisions in order to maximize own fitness. The developmental potential is linked to the moulting interval, as only individuals in the sensitive phase are able to react to a changing situation like orphaning. Thus the sensitive phase, besides honest signalling (via cuticular hydrocarbon profiles and trophallaxis) might be an further mechanism potentially regulating conflict in C. secundus, as it restricts the number of individuals capable of becoming neotenic in a ‘fair lottery’ process.