Human endogenous retroviruses (HERVs) are viral “fossils” in the human genome that originated from the ancient integration of exogenous retroviruses. Although HERVs have sporadically been reported in nonhuman primate genomes, their deep origination in pan-primates remains to be explored. Hence, based on the in silico genomic mining of full-length HERVs in 49 primates, we performed the largest systematic survey to date of the distribution, phylogeny, and functional predictions of HERVs. Most importantly, we obtained conclusive evidence of nonhuman origin for most contemporary HERVs. We found that various supergroups, including HERVW9, HUERSP, HSERVIII, HERVIPADP, HERVK, and HERVHF, were widely distributed in Strepsirrhini, Platyrrhini (New World monkeys) and Catarrhini (Old World monkeys and apes). We found that numerous HERVHFs are spread by vertical transmission within Catarrhini and one HERVHF was traced in 17 species, indicating its ancient nature. We also discovered that 164 HERVs were likely involved in genomic rearrangement and 107 HERVs were potentially coopted in the form of noncoding RNAs (ncRNAs) in humans. In summary, we provided comprehensive data on the deep origination of modern HERVs in pan-primates.