Social insects have developed a broad diversity of nesting and foraging strategies. One of these, inquilinism, occurs when one species (the inquiline) inhabits the nest built and occupied by another species (the host). Obligatory inquilines must overcome strong constraints upon colony foundation and development, due to limited availability of host colonies. To reveal how inquilinism shapes reproductive strategies in a termite host‐inquiline dyad, we carried out a microsatellite marker study on Inquilinitermes inquilinus and its host Constrictotermes cavifrons. The proportion of simple, extended and mixed families was recorded in both species, as well as the presence of neotenics, parthenogenesis and multiple foundations. Most host colonies (95%) were simple families and all were monodomous. By contrast, the inquiline showed a higher proportion of extended (30%) and mixed (5%) families, and frequent neotenics (in 25% of the nests). This results from the simultaneous foundation in host nests of numerous incipient colonies, which, as they grow, may compete, fight, or merge. We also documented the use of parthenogenesis by female–female pairs. In conclusion, the classical monogamous colony pattern of the host species suggests uneventful development of simple foundations dispersed in the environment, in accordance with the wide distribution of their resources. By contrast, the multiple reproductive patterns displayed by the inquiline species reveal strong constraints on foundation sites: founders first concentrate into host nests, then must attempt to outcompete or absorb the neighbouring foundations to gain full control of the resources provided by the host nest.