Plants adapt to abiotic stresses by a variety of physiological and molecular mechanisms, among which the root plays important roles via responding to underground and soilborne signals. Fructan is a polysaccharide involved in energy metabolism and stress adaptation. Orobanche cumana is a holo-parasitic plant that mainly attaches to the root of the host sunflower (Helianthus annuus). Oc6-FEH, a fructan 6-exohydrolase from O. cumana, is involved in both fructan metabolism and flooding responses. Expression of Oc6-FEH is induced by flooding and indole-3-acetic acid (IAA). Oc6-FEH possesses fructan catabolism activity and is associated with fructose release. Overexpression of Oc6-FEH in the host sunflower reduces malondialdehyde (MDA) and hydrogen peroxide (H₂O₂) accumulation, boosts the activities of antioxidant enzymes, including peroxidase (POD) and superoxide dismutase (SOD), and enhances photosynthetic performance. The expression level of Oc6-FEH was found to be positively associated with the flooding tolerance of invading O. cumana, which is connected to the host root. Furthermore, IAA treatment also improved the flooding tolerance of O. cumana. In summary, the metabolism of fructan and the activity of Oc6-FEH were demonstrated to ameliorate waterlogging stress. Oc6-FEH provides a promising genetic target for the improvement of flooding tolerance in crops.