The Origin Recognition Complex (ORC) plays a central role in determining the initiation sites of DNA replication in eukaryotes. In higher eukaryotes, ORC lacks sequence-specific DNA binding and the mechanisms of ORC recruitment and origin determination are poorly understood. ORC is recruited with high efficiency to the Epstein-Barr Virus (EBV) origin of plasmid replication (OriP) through a complex mechanism involving interactions with the virus-encoded EBNA1 protein and human TRF2. We mapped the regions of EBNA1 necessary for OriP ORC recruitment and replication to the RGG-like motifs LR1 and LR2. These regions also confer metaphase attachment ability to EBNA1. We found that LR1 and LR2 recruitment of ORC is RNA-dependent and requires a subdomain of Orc1. HMGA1a, which can functionally substitute for the RGG domains, also recruits ORC in an RNA-dependent manner. EBNA1 and HMGA1a RGG motifs, as well as the Orc1 subdomain, bind to structured G-rich RNA. RNase A treatment of cellular chromatin released a fraction of total ORC, suggesting that ORC association with chromatin, and possibly cellular origins, is stabilized by RNA. We characterized the RNA responsible for EBNA1 interaction with ORC and showed that it is RNA capable of forming G-quadruplex structures. Drugs that specifically interact with G-quadruplex structures decrease EBV-positive cell viability. This may be due to the requirement of G-quadruplex structures in EBNA1-dependent replication at DS as well as metaphase attachment during cellular division. Furthermore, we showed that TRF2 interacts with the same subdomain of Orc1 as EBNA1. The recruitment of ORC by TRF2 to both OriP and telomeres is also RNA-dependent and mediated by the TERRA RNA, which is capable of forming G-quadruplexes. We propose that structural RNA molecules mediate ORC recruitment at OriP as well as some cellular origins.