Control of the crop pest African cotton leafworm Spodoptera littoralis (Boisduval) by chemical insecticides has led to serious resistance problems. Ajuga plants contain phytoecdysteroids (arthropod steroid hormone analogs regulating metamorphoses) and clerodanes (diterpenoids exhibiting antifeedant activity). We analyzed these compounds in leaf extracts of the Israeli Ajuga iva L. by LC-TOF-MS and TLC, and their efficiency at reducing S. littoralis fitness. First and third instars of S. littoralis larvae were fed on castor bean leaves smeared with an aqueous suspension of dried methanolic crude extract of A. iva phytoecdysteroids and clerodanes. Mortality, larval weight gain, relative growth rate and survival were compared to feeding on control leaves. We used DAPI and phalloidin staining to localize A. iva crude leaf extract activity in the insect gut. A. iva crude leaf extract (50, 100 and 250 µg/µL) significantly increased mortality of first-instar S. littoralis larvae (36%, 70% and 87%, respectively) compared to controls (6%). Third-instar larval weight gain decreased significantly (by 52%, 44% and 30%, respectively), as did relative growth rate (–0.05 g/g per day compared to the relevant controls), ultimately resulting in few survivors. Crude leaf extract (250 µg/µL) reduced gut size, with relocation of nuclei and abnormal actin-filament organization. A. iva extract has potential for alternative, environmentally safe insect-pest control.