The evolution of insects inhabiting arid environments is heavily shaped by resource scarcity and temperature. Ecological interdependence could be tight and complex as in the model cactus–yeast–Drosophila. Cactophilic species of Drosophila (Diptera: Drosophilidae) differ in their preference for the type of breeding resources and life‐history traits that respond to variation in environmental temperature. Adult flies feed and breed on rotting cacti but they are physiologically limited to cope with temperature changes. However, flies can behaviourally avoid such stressful conditions by actively seeking benign microhabitats. We investigate how alternative breeding resources (cactus species) and thermal environment affect the spontaneous adult locomotor activity in two species, Drosophila buzzatii Patterson & Wheeler and Drosophila koepferae Fontdevila & Wasserman, adapted to semi‐arid environments. Locomotor activity of D. buzzatii was more affected by the breeding resource, whereas D. koepferae showed a clear ‘bell shape’ activity curve in response to a wide range of temperatures, independent of the breeding resource. These idiosyncratic responses suggest that the selective pressures that shaped life‐history evolution in these Drosophila species were different, with the breeding resource and environmental temperature contributing to the development of diverging survival strategies in arid environments.