Flavonoids are involved in many physiological processes in plants. TRANSPARENTTESTA 4 (TT4) acts at the first step of flavonoid biosynthesis, and the loss of TT4 function causes a lack of flavonoid. Flavonoid deficiency is reportedly the main causeof increased fatty acid content in pale‐coloured oilseeds, but details regarding therelationship between seed flavonoids and fatty acid biosynthesis are elusive. In thiswork, we applied a genetic strategy combined with biochemical and cytological assaysto determine the effect of seed flavonoids on the biosynthesis of fatty acids in Arabidopsis thaliana. We showed that TT4‐mediated flavonoids negatively affectembryonic fatty acid biosynthesis. A crossing experiment indicated that seedflavonoid biosynthesis and the impact of this process on fatty acid biosynthesis werecontrolled in a maternal line‐dependent manner. Loss of TT4 function activatedglycolysis in seed embryos, thereby enhancing fatty acid biosynthesis, but did notimprove seed mucilage production. Moreover, loss of TT4 function reduced PIN‐FORMED 4 expression and subsequently increased auxin accumulation in embryos. Pharmacologically and genetically elevated auxin levels enhanced seed fatty acidbiosynthesis. These results indicated that flavonoids affect fatty acid biosynthesisby carbon source reallocation via regulation of WRINKLE1 and auxin transport.