Cuscuta campestris is a parasitic weed species with noxious effects in broadleaf crops worldwide. The control of Cuscuta in the majority of crops affected is limited or non-existing. We tested, for the first time, the effect of eighteen metabolites in in vitro-grown Cuscuta seedlings. We found that 2-benzoxazolinone, hydrocinnamic acid and pisatin caused the strongest inhibition of seedling growth. In addition to seedling growth, pisatin caused necrosis of the Cuscuta seedling, occurring mostly at the seedling shoot. Scopoletin and sesamol treatments caused toxicity, observed as a black staining, only at the Cuscuta root apices, while caffeic acid, ferulic acid and vanillic acid caused toxicity, observed as brown staining, in the root apices. The structure–activity relationships in four structural derivatives of 2-benzoxazolinone, and five structural derivatives of hydrocinnamic acid, were also studied. The identification of new herbicidal modes of action against Cuscuta is the first step in creating new alternatives to sustainable chemical control of parasitic weeds.