ETS1 is the archetypal member of the metazoan ETS transcription factor family. All the members of this family bind to the conserved GGA(A/T) core ETS binding sequence (EBS). Several ETS family members exhibit autoinhibition, wherein one domain of ETS blocks its own DNA-binding activity until certain conditions are met. Relief of autoinhibition in these proteins is coupled to homo- or hetero-dimer formation. Relief of autoinhibition in full-length ETS1 is catalyzed by non-specific interaction with DNA, which facilitates the formation of protein dimers. The ETS1 splice variant, ETS1-p42, lacks an exon that encodes a crucial part of the autoinhibitory module. Thus, ETS1-p42 does not autoinhibit. We showed that the absence of autoinhibition allows ETS1Δ335, an N-terminal deletion that recapitulates the DNA- binding of ETS1-p42, to form homodimers in the absence of DNA. However, ETS1-p42 is thought to bind its DNA sites only as monomers. Here, we explore this paradox and show that ETS1Δ335 binds cooperatively to DNA containing two EBSs. We also show that residues in ETS1DNA recognition helix mediate this DNA-binding cooperativity. Furthermore we also find that a single EBS can bind two ETS1Δ335 subunits. Finally, we show that DNA acts catalytically to separate unbound ETS1Δ335 dimers into monomers. Together, these results suggest a model of ETS1-p42 DNA-binding, where ETS1-p42 can bind to a single EBS with 2:1 stoichiometry.