The transition from oocyte-to-embryo is a dramatic process in which the previously quiescent oocyte undergoes a series of highly coordinated events that lead to maturation, fertilization, and initiation of mitotic divisions. In the nematode Caenorhabditis elegans, this process occurs rapidly and continuously when reproductive maturity is reached. In the short time between fertilization and the first mitotic division, the C. elegans embryo completes meiosis, establishes a polarity axis critical for development, and forms a complex multilayered eggshell. A growing body of evidence indicates that de novo lipid synthesis and lipid modification are critical for these early embryonic events. Here, we demonstrate the central role that the C. elegans holocarboxylase synthetase, BPL-1 performs in fatty acid de novo synthesis and in the early embryo. Mutations in the bpl-1 gene are maternal-effect lethal, and cause defects in PAR polarity, meiosis, and synthesis of the eggshell permeability barrier. We found that a major consequence of disrupting BPL-1 and other de novo synthesis genes was a change in fatty acid composition, specifically, a large decrease in polyunsaturated fatty acids (PUFAs). The decrease in PUFAs was much greater in embryos than in the parent, suggesting that maintenance of embryonic fatty acid composition is more dependent on the lipid biosynthesis machinery than the soma. We provide evidence that dietary malonyl-CoA and biotin support de novo synthesis in the whole worm, but not in the embryo, which helps to explain the greater need for de novo lipid synthesis machinery in embryos. Further, analysis of fatty acid desaturase mutants demonstrates that PUFAs contribute to synthesis of the embryonic permeability barrier and completion of meiosis. Our evidence supports a model in which dietary and de novo synthesized malonyl-CoA converge to support de novo synthesis of fatty acids and maintenance of lipid composition in C. elegans, but in the sequestered environment of the early embryo, dietary support is unavailable, increasing the importance of the fatty acid de novo synthesis machinery to maintain fatty acid composition and to synthesize the specific lipids required in the embryonic permeability barrier.