In order to maintain organismal fitness, the germline must be able to transmit high-fidelity genomic information from one generation to the next. Transposable Elements (TEs), genomic elements which are capable of mobility within the genome, pose a risk to this process. Within a given species, only a small subset of TEs remain mobile. These mobile elements are often evolutionarily young compared to others in the genome and must be durably silenced during germline development so that their mobility does not impact fitness of the offspring. Conversely, evolutionarily older TEs lose their ability to mobilize due to deterioration or loss of pro-viral regions, which encode viral proteins. In tandem with their deterioration, TEs are often “endogenized” or “domesticated” and become cis-regulatory elements, for instance by harboring binding motifs of transcription factors, repressors, or insulators. As a result, a conserved property of these TEs is their capacity to embed themselves into the cis-regulatory network of tissues, especially in the early embryo. Primordial Germ Cells (PGCs) are embryonic precursors to the adult germline. In mammals, PGCs are specified early in embryonic development ( at embryonic day (E) E6.25 in mice and ~E11-12 in humans). The transcriptional networks that drive and reinforce acquisition of PGC identity have been well interrogated using in vitro models of PGC specification in the mouse (m) and human (h) via generation of PGC-Like Cells (PGCLCs). Here we show that an evolutionarily young TE subfamily, LTR5Hs, is epigenetically remodeled during human PGC specification and bound by critical human PGC factors, supporting the hypothesis these elements act as enhancers. We go on to show that ectopic epigenetic repression of LTR5Hs results in inefficient human PGCLC induction, thus establishing enhancer activity of LTR5Hs as necessary for human PGC specification. These findings demonstrate that LTR5Hs is necessary for specification of the human germline. After specification, PGCs will migrate while undergoing epigenetic reprogramming including DNA demethylation and imprint erasure. In the mouse, PGCs migrate into the developing genital ridge, undergo rapid mitotic proliferation and differentiate into either testicular germ cells, which become pro-spermatogonia, or into meiotic germ cells which will undergo meiosis and mature into oocytes. To ask how control of TEs impacts a later stages of PGC development, differentiation, we used an in vivo mouse model and employed PGC-specific conditional knockout of TRIM28. TRIM28 is an epigenetic scaffold necessary to repress many TEs, especially those which are evolutionarily young. We found that TRIM28 is regulated in a sex-specific manner and that TRIM28 loss in PGCs during differentiation results in upregulation genes typical of Zygotic Genome Activation, which in the mouse happens during the 2C stage of embryonic development. Upregulation of a 2C-like transcriptome results in reduced mitotic expansion, inefficient fate restriction to the adult germline, and a failure of PGCs to differentiate in males and to properly progress through meiosis in females. Thus, precise control of transposable elements is important not only for germline specification, but also to protect the germline transcriptional program as PGCs differentiate.