Human single stranded DNA binding protein 1 (hSSB1) has been found to play a central role in double stranded break (DSB) repair by homologous recombination, and more recently, in the removal of mutagenic 8-oxo-7,8-dihydro-guanine (8-oxoG) from the genome through Base Excision Repair (BER). While hSSB1 acts as a functional monomer under reduced conditions, we have found that the ability of hSSB1 to form disulfide bond linked dimers, tetramers and higher oligomers under oxidative conditions is critical to its function in BER. In this work we use NMR and SPR experiments to determine how oligomeric hSSB1 binds ssDNA and ssDNA incorporating 8-oxoG bases. Our findings reveal that binding of oxidised hSSB1 to 8-oxoG ssDNA is indistinguishable to its binding to unmodified ssDNA, indicating no change in the underlying base-stack mechanism. Further, using SPR we show that oxidised hSSB1 binds stronger to ssDNA than reduced protein confirming that hSSB1 oligomers recognise ssDNA with a tighter binding affinity. To determine the structural basis of these oligomeric hSSB1-ssDNA interactions we carried out NMR HSQC titrations with ssDNA oligos of varying length. Our data reveal that ssDNA binding takes place via hSSB1 dimers and tetramers that are structurally identical to the ones that we previously described in the absence of ssDNA.