In some social insects, workers can produce females asexually through thelytokous parthenogenesis. This allows them to produce replacement queens (i.e. requeening) if the queen has died, but also to compete with the queen to produce females (i.e. reproductive cheating). For the first time, we experimentally tested the role of worker thelytoky under quasinatural conditions in the ant Cataglyphis cursor, where the queen uses both sexual and thelytokous reproduction. We reared pairs of orphaned and queenright colonies in enclosures for almost 3 months, during which they competed for resources. Orphaned colonies lost more workers than queenright colonies over the course of the experiment, presumably because of the costs of reproductive conflicts between workers. Nevertheless, they produced new queens through worker thelytoky and new colonies through colony fission. This is the first unambiguous demonstration that worker thelytoky allows requeening under natural conditions in this species. We further showed that worker thelytoky results in reproductive cheating in the form of a few workers reproducing in the presence of the queen (in queenright colonies) and a few worker lineages producing more new queens than other lineages (in orphaned colonies). In addition, it also results in rare instances of social parasitism, that is, workers entering and reproducing in foreign colonies. These benefits to workers seem too occasional and too low to drive the evolution of thelytoky in this species. We argue that thelytoky probably evolved in the queen caste, where it allows the production of young queens and confers frequent and large benefits by increasing gene transmission, but is also expressed in workers because of genetic correlations between the two castes.