In sheep, the presence of the Booroola F gene has several important consequences for ovarian function. This study investigated the consequences of the presence of the F gene for the insulin-like growth factor (IGF) system in the ewe ovary. Studies were undertaken in ovaries from F and Mérinos d'Arles ewes to determine 1) the levels of type I IGF receptors and IGF binding proteins (IGFBPs) in follicular cells by quantitative autoradiography of [¹²⁵]-IGF-I binding sites on ovarian sections; 2) the pattern of intrafollicular IGFBPs, by Western-ligand blotting on follicular fluids; and 3) the effects of IGF-I and FSH on proliferation and differentiation of granulosa cells in vitro, assessed by progesterone secretion and cytochrome P450 side-chain cleavage (P450_scc) expression. The amounts of type I IGF receptors were similar in F and follicular cells; however, at the same follicular size, F healthy follicles contained lower concentrations of IGFBPs smaller than 40 kDa (particularly IGFBP-2) than healthy follicles. In vitro, in basal conditions as well as in IGF-I- or FSH-stimulated conditions (or both), granulosa cells from F follicles had a lower proliferative activity, secreted higher amounts of progesterone, and expressed higher levels of P450_scc than granulosa cells from follicles of the same size. When F and preovulatory follicles were compared at the end of the follicular phase, IGFBPs <40 kDa concentrations were slightly higher, and responsiveness of granulosa cells to FSH in vitro was lower in F than in follicles, suggesting that terminal maturation of F follicles, although precocious, was less complete than it was in follicles. The early decrease in intrafollicular IGFBPs <40 kDa concentrations observed in F antral follicles, which likely leads to an early increase in IGF bioavailability, may at least partly account for the increased ovulation rate that characterizes F-carrier ewes.