This study examined whether the low body-fat reserves in sheep with high estimated breeding values (EBVs) for clean fleece weight (CFW) reported previously are affected by nutritional history, and second whether the effect may be related to differences in the variation in fibre diameter (CVfd). Groups of 11 20-month-old Merino ewes with high and low EBVs for CFW and for CVfd were compared in a 2 × 2 design at low bodyweight, then fed ad libitum for 100 days and re-measured. The response of wool growth rate to feed supply (WRF) was estimated as the slope of the regression against time of clean wool mass collected from mid-side patches at intervals of 30–40 days throughout the experiment. High CFW sheep had greater feed intake relative to liveweight and liveweight gain (P = 0.02), but did not differ significantly in other characteristics from low CFW sheep. High CVfd sheep had lower plasma concentrations of insulin (P = 0.02), IGF-1 (P = 0.03), and albumin (P = 0.02) throughout the study, and had less fat when in poor body condition (P = 0.02). The WRF was greater in both the high CFW (P = 0.003) and the high CVfd (P = 0.004) genotypes. When studied in poor body condition, sheep with a high WRF had lower liveweight (P < 0.001), lower body condition score (P < 0.001), lower plasma albumin (P < 0.001), and higher plasma growth hormone (P = 0.02), but these relationships weakened or disappeared after ad libitum feeding. Sheep with high WRF also had lower plasma concentrations of insulin (P = 0.002) and IGF-1 (P = 0.008) throughout the study, which may have brought about the increased responsiveness of protein and energy metabolism to nutrition. The results indicate that genetic selection for wool characteristics can affect the responsiveness of wool growth rate to nutrient supply. Sheep that are highly responsive grow more wool when offered abundant feed, but may have lower body nutrient reserves when on limited feed.