Circoviruses are ubiquitous and can infect a wide range of mammal and avian hosts. The replication associated protein (Rep) from these viruses is responsible for initiating genome replication using the rolling circle replication (RCR) mechanism. Rep carries out this function through its two functional domains, an endonuclease domain, and a helicase domain, responsible for nicking and ligating ssDNA and unwinding double-stranded DNA (dsDNA). The aim of this study was to recombinantly express Beak and feather disease virus (BFDV) Rep in E. coli and solve the high-resolution structure of Rep through cryo-EM. The structure demonstrates full-length Rep assembles in a hexameric ring similar to that of the viral helicases from the superfamily 3 (SF3) of ATPases Associated with diverse cellular Activities (AAA+). Further 3D classification and refinement has allowed two conformations of the complex to be resolved at 3.4 and 3.7 Å resolution and a model for the full Rep complex. Analysis of the structure has shown the presence of an oligonucleotide loaded on the helicase domain and allowed the identification of three residues implicated in this interaction. The significance of these residues has been tested by the production and purification of point mutants to further probe its capacity for ssDNA binding and replication. This information is important for defining the molecular mechanisms that underlie their functions and would also open new avenues for the design of new antiviral strategies against these viruses.