The common fig bears a unique closed inflorescence structure, the syconium, composed of small individual drupelets that develop from the ovaries, which are enclosed in a succulent receptacle of vegetative origin. The fig ripening process is traditionally classified as climacteric; however, recent studies have suggested that distinct mechanisms exist in its reproductive and non-reproductive parts. We analysed ABA and ethylene production, and expression of ABA-metabolism, ethylene-biosynthesis, MADS-box, NAC, and ethylene response-factor genes in inflorescences and receptacles of on-tree fruit treated with ABA, ethephon, fluridone, and nordihydroguaiaretic acid (NDGA). Exogenous ABA and ethephon accelerated fruit ripening and softening, whereas fluridone and NDGA had the opposite effect, delaying endogenous ABA and ethylene production compared to controls. Expression of the ABA-biosynthesis genes FcNCED2 and FcABA2, ethylene-biosynthesis genes FcACS4, FcACOL, and FcACO2, FcMADS8, 14, 15, FcNAC1, 2, 5, and FcERF9006 was up-regulated by exogenous ABA and ethephon. NDGA down-regulated FcNCED2 and FcABA2, whereas fluridone down-regulated FcABA2; both down-regulated the ethylene-related genes. These results demonstrate the key role of ABA in regulation of ripening by promoting ethylene production, as in the climacteric model plant tomato, especially in the inflorescence. However, increasing accumulation of endogenous ABA until full ripeness and significantly low expression of ethylene-biosynthesis genes in the receptacle suggests non-climacteric, ABA-dependent ripening in the vegetative-originated succulent receptacle part of the fruit.