Understanding the causes of the exceptional rate of evolution of the mammalian placenta is likely to aid the understanding of placental development and the aetiology of the human specific pregnancy disorder pre-eclampsia (PE). As a set of transposable elements (TE) are often lineage-specific and known to be co-opted for placental functioning, here we consider the TE binding partners of GATA3 and DLX5 that govern trophectoderm regulatory networks and have previously been shown to be grossly dysregulated in PE. This identifies a set of TEs, including the endogenous retroviral (ERV) LTR8B. LTR8B and another ERV, MER65, are enriched at the multigene pregnancy-specific glycoprotein (PSG) gene array, a recently amplified, highly intra-specifically variable and dynamic primate specific genomic region. We find that both LTR8B and MER65 contribute to the evolution of the PSG genes and their functional diversification from the related membrane bound CEACAM gene family. MER65 elements promoted the initial evolution of secreted PSG variants by providing alternative polyA signal(s) of a truncated C terminus protein, ablating the transmembrane domain. By contrast, the LTR8B promoter/enhancer provides differential binding of transcription factors (TFs) (e.g. GATA2/3, DLX5, TFAP2A/C) and defines a diversified expression pattern of the PSG genes. CRISPR-Cas9 knockouts, expression rescue and 3D chromatin studies reveal that while LTR8B copies were co-amplified along with the PSG genes, PSG9 is exceptional. The LTR8B/PSG9 promoter/enhancer controls additional PSG members, trophoblast-specific TFs and several key pregnancy genes. This LTR8B/PSG9 governed regulatory network plays a central role in differentiation of the multinucleated syncytiotrophoblast. Dysregulation of GATA3 is associated with elevated levels of PSG9 in the maternal serum of PE patients in the first trimester, holding promise for the development of a predictive biomarker. We conclude that PSG9 represents an instance of taxonomically restricted TE recruitment for placental function with dysregulation associated with human-specific preeclampsia.