Mating flights take place in the Chihuahuan desert in July, in the evening, around 6:00-7:00 PM. The mating flight is a mating system wherein both the prospective queens and the males, all of which have wings, take flight and mate while airborne. The males die immediately following this copulatory flight, while the females land and quickly lose their wings. Fertilized queens may be found on the ground around 30 minutes later, at which point they wander around and try to find sites for nests. This one mating flight will provide the queen with all of the sperm she will need for her entire life, and she will spend the rest of her life in the nest, laying eggs (Holldöbler & Carlin, 1989: 132).

The queens of Aphaenogaster cockerelli lay eggs that may be either male, female (reproductive queen), or female (worker). The eggs are oval, firm and white, and are taken care of by the workers. The eggs hatch into larvae, which are also small and white. The larvae eventually become adult ants. The female workers can also lay unfertilized, viable eggs in the absence of the queen, but these hatch into males only. Males and queen females are only produced by the queen once a year for the mating season. Worker females are produced year-long (Holldöbler & Carlin, 1989: 140).

As the males die subsequent to the mating flight, all of the raising of young is carried out by the queen and the workers. The queen is the only individual in the colony that lays viable eggs. This is not because the workers are incapable of laying viable eggs, but instead because the queen inhibits their egg production with pheromones, possibly imbued in the casings of the eggs she lays. The exact mechanism is not known for this species. The workers are in fact capable of laying viable eggs, and in situations where the queen is absent from the colony, they will do so, though these eggs will invariably hatch into males only, so the colony is ultimately doomed. Normal egg production in workers (in colonies for which the queen is present) is limited to trophic eggs. These are non-viable eggs created solely to be eaten by the queen, larvae, and other workers.

Eggs and larvae are taken care of by the workers. Eggs are collected into egg piles, which are then tended (grooming) and protected by the workers. Larvae hatch out of the eggs, and continue to be taken care of by the workers. They are moved around and guarded. They are fed droplets of liquid which are produced by the workers, as well as foraged food pieces and oral glandular secretions, which are passed mouth-to-mouth. Larvae eventually become workers, and at that point are mature adults (Holldöbler & Carlin, 1989: 135).