So far, the three-dimensional (3D) folded structure of a protein has been considered essential for its function(s). However, recently many proteins have been identified to function without having a definite structure and they are classified as intrinsically disordered proteins. These proteins lack a single folded conformation, instead, they have a dynamically interconverting ensemble of structures either of the whole or parts of the protein. Recently, we have identified and structurally characterized a βγ-crystallin domain (named as Hahellin) in the genome of a marine bacterium called Hahella chejuensis on the basis of sequence signature of a βγ-crystallin. This protein has been characterized by NMR spectroscopy as an intrinsically disordered protein, which upon Ca2+-binding undergoes a large conformational transformation and acquires a typical βγ-crystallin fold. In this paper, we have characterized the intrinsically disordered state of Hahellin by NMR and Replica Exchange Molecular Dynamics (REMD) simulations and found it to be in a highly flexible molten globular state with a relatively structured N-terminal Greek key motif. Network analysis and clustering on the observed conformational ensemble show a heterogeneous mixture of multiple conformations. Many of the observed conformational clusters display an increased helical propensity and decreased β-strand propensity as compared to the protein in the Ca2+-bound state, consistent with observations made on the Ca2+-free state of the protein by NMR. The clusters with larger populations show 50-60% native contacts in their structural topology, similar to that of the Ca2+-bound form of Hahellin, while the rest show a completely altered conformational states. Taken together, this study provides an in-depth understanding of conformational dynamics and therefore the function of the intrinsically disordered protein.