DNA chemical modifications are being explored for identifying potential drug targets, but it remains a challenging task. In our study, we introduced double-methylated guanosine into a DNA duplex and employed NMR and restrained molecular dynamics to determine its structure in solution. The incorporation of double-methylated guanosine led to the formation of an aberrantly distorted Z-DNA with an expanded groove space. This newly formed flexible Z-DNA exhibited slow conformational changes occurring on the timescale of seconds and adopted a unique helical structure, which we refer to as the tBZ-form. Our investigation of the Z-to-tBZ transition revealed three key features. First, the transition involved a shift from the syn-to-syn glycosidic conformation, transforming the DNA from a Z-DNA to a non-B-DNA form. Second, the left-handed helical nature of Z-DNA was lost during the transition, resulting in a non-Z-DNA structure. Lastly, the Z-to-tBZ transition was accompanied by an entropic gain. Based on our findings, we propose that this flexible Z-DNA represents a promising target for drug discovery. Moreover, the Z-to-tBZ transition offers valuable insights into the structural diversity of DNA, potentially opening new avenues for further exploration.