Protein disorder is prevalent in proteins which are involved in DNA binding, such as transcription factors. Transcription factors commonly contain disorder within protein-protein interaction interfaces, however a small number of families contain disorder in their DNA binding domain such as the basic leucine zipper proteins (bZIP). bZIP proteins like cAMP response element binding protein (CREB) have a wide range of roles in human health, however the role of disorder in how bZIP proteins find their cognate DNA site within the nucleus is still unknown. In addition, significant controversy exists about whether bZIP proteins search for the target as a preformed dimer or by sequential association of monomers. Using a range of biophysical techniques including stopped flow kinetics and nuclear magnetic resonance spectroscopy with constructs to mimic the monomer or dimer species, this question has been examined. The CREB homodimer affinity was found to be high, at the upper limit of what had been previously seen for bZIPs. CREB is able to recognise the cognate DNA CRE motif specifically as a preformed dimer and undergoes coupled folding upon binding. In the search mode, however, the basic region remains dynamic with more disordered character. Compared to the dimeric construct, a monomeric CREB model exhibited a lack of specificity for the cognate site and several orders of magnitude reduction in affinity. The affinity for DNA by the monomer appears to be dependent on the propagation of helical content into the DNA-binding basic region, which directly contacts the DNA, from the leucine zipper in the dimer. CREB bZIP also searches for its target DNA using a combination of intersegmental transfer and sliding, with the residual helical content in the basic region controlling these rates. CREB therefore appears to perform effective target search preferentially through the pre-formed dimer pathway, independent of the presence of excess competitor DNA which is consistent with the homodimer stability, but can also proceed through the monomer pathway albeit with a reduced affinity for the target. This work therefore extends our understanding towards describing the target search mode and mechanism by a disordered transcription factor.