In ant–plant protection mutualisms, plants provide nesting space and nutrition to defending ants. Several plant–ants are polygynous. Possessing more than one queen per colony can reduce nestmate relatedness and consequently the inclusive fitness of workers. Here, we investigated the colony structure of the obligate acacia-ant Pseudomyrmex peperi, which competes for nesting space with several congeneric and sympatric species. Pseudomyrmex peperi had a lower colony founding success than its congeners and thus, appears to be competitively inferior during the early stages of colony development. Aggression assays showed that P. peperi establishes distinct, but highly polygynous supercolonies, which can inhabit large clusters of host trees. Analysing queens, workers, males and virgin queens from two supercolonies with eight polymorphic microsatellite markers revealed a maximum of three alleles per locus within a colony and, thus, high relatedness among nestmates. Colonies had probably been founded by one singly mated queen and supercolonies resulted from intranidal mating among colony-derived males and daughter queens. This strategy allows colonies to grow by budding and to occupy individual plant clusters for time spans that are longer than an individual queen’s life. Ancestral states reconstruction indicated that polygyny represents the derived state within obligate acacia-ants. We suggest that the extreme polygyny of Pseudomyrmex peperi, which is achieved by intranidal mating and thereby maintains high nestmate relatedness, might play an important role for species coexistence in a dynamic and competitive habitat.