Human endogenous retrovirus type-H (HERVH) is specifically expressed in the pluripotent stem cells of the pre-implantation embryo. A subset of these elements appear to exert regulatory activities promoting pluripotency and self-renewal. How HERVH attained this specific expression pattern and incorporated itself into the human pluripotency network has not been revealed. In the first part of this dissertation, we aimed to elucidate the sequence features responsible for HERVH pluripotent transcription. We performed a “phyloregulatory” analysis of the long terminal repeat (LTR7) sequences, which harbors HERVH’s promoter, in which we layered genomic regulatory data onto a phylogenetic tree of LTR7 sequences. The results showed that LTR7 consists of at least 8 previously undefined subfamilies with unique evolutionary histories, transcription factor binding site (TFBS) profiles, and embryonic transcriptional niches. Only one of the youngest LTR7 subfamilies, we term 7up, exhibited promoter activity in pluripotent stem cells. We found that a complex series of deletions, duplications, and recombination events, led to the emergence of a cis-regulatory module unique to 7up, which is necessary for 7up’s pluripotent promoter activity. Together, these data highlight the unexpected role of inter-element recombination in driving the mosaic cis-regulatory evolution of an endogenous retrovirus. In the second part of this dissertation, we focused on the regulatory effects of intra-element recombination between the LTRs of HERVH. Intra-element recombination is a common mechanism by which a full-length endogenous retrovirus with two LTRs and coding genes collapses into one solitary (solo) LTR. We hypothesized that the full-length to solo transition may result in changes in an element’s regulatory properties. To test this hypothesis, we compared the regulatory activity of solo and full-length LTR7up. We found that only full-length loci exhibit pluripotent promoter activity, while solo loci generally exhibited the hallmarks of active enhancers. Comparative genomics revealed the formation of solo LTR7 via recombination has occurred continuously throughout hominoid evolution, uncovering a potent mechanism of cis-regulatory variation in humans and great apes. This dissertation reveals the impact of both inter- and intra-element recombination in the evolution of regulatory DNA in the primate genome.