The biosynthesis of the major lipids of photosynthetic membranes, i.e. monogalactosyldiacylglycerol (MGDG) and digalactosydiacylglycerol (DGDG), occurs in the envelope of chloroplasts. In Angiosperms two enzymes of the galactolipid biosynthesis pathway are localized in the inner envelope membrane (IEM), i.e. a phosphatidic acid phosphatase (PAP), which dephosphorylates phosphatidic acid (PA) into diacylglycerol (DAG) and MGD1, catalyzing the galactosylation of DAG, thus generating MGDG. MGD1 is the main MGDG synthase in green tissues of Arabidopsis, responsible for the massive synthesis of galactolipids required for thylakoid expansion. In vitro studies support the existence of both a negative regulation of the plastid PAP by DAG and an activation of MGD1 by PA. As an alternative to the synthesis of DAG and PA in the IEM, these precursors can be diverted from extraplastidial phospholipids after hydrolysis by phospholipases. The tuning of galactolipid synthesis by PA and DAG could possibly be one of the most critical regulatory processes of membrane lipid homeostasis at the whole cell level. We developed a simple mathematical model of the chloroplast IEM galactolipid biosynthesis pathway, without any prior conception of the expected dynamical behaviour, in order to understand the enzymatic behaviors implied by the regulatory motifs revealed by experimentations. We used parameters obtained by experimental enzymatic studies for numerical simulations. We first demonstrated that the existence of these regulatory motifs imply the establishment of stationary states for PA and DAG. The system also implies that PA can accumulate and be used for alternative pathways such as PG synthesis. A massive influx of eukaryotic PA appears unlikely whereas an influx of eukaryotic DAG in the IEM is possible with an orientation of this precursor toward a rapid synthesis of MGDG. The model also implies that DAG cannot accumulate and that the influx of PA acts as a determinant signal switching the whole system on. Eventually, the dynamic property of the system can precede a loss of the PAP enzyme, an evolutionary event that occurred independently in the majority of Angiosperm clades, with little changes in the overall metabolic fluxes.