The basic Helix-Loop-Helix-Per-Arnt-Sim (bHLH-PAS) transcription factors (TFs) are regulators of several critical cellular functions such as circadian rhythm, hypoxia response and neuronal development. These proteins contain tandemly repeated PAS domains that mediate heterodimer formation. While PAS domains adopt a conserved fold, recent studies suggest that their interaction interfaces differ distinctly in different TF complexes. However, the implications of these differences on the intrinsic dynamics of PAS domains remain unclear. In this study, we performed a comparative analysis of PAS domain dynamics across multiple bHLH-PAS TF complexes using all-atom Elastic Network Models (ENMs) and molecular dynamics (MD) simulations. We decomposed the intrinsic dynamics of PAS domains into self-coupled (internal domain dynamics) and directly coupled (interaction partner-influenced dynamics) motions using a projection-based approach. Our results show that self-coupled motions are more conserved across PAS domains than structure or sequence alone, while directly coupled motions capture the context-specific influence of partner proteins. Furthermore, hierarchical clustering of the overall covariance-based similarity scores revealed distinct grouping of CLOCK:BMAL1-type and HIF:ARNT-type complexes, which were not captured by sequence or structural comparisons. Root mean square fluctuation profiles derived from both MD and ENM approaches showed strong correspondence, validating the utility of ENMs in capturing biologically relevant dynamics, even in cases where the structural complexes were modelled using AlphaFold3. PAS-B domains were generally found to be less flexible than PAS-A domains for all the complexes analysed. Regions with high directly coupled flexibility were generally localized regions with high interface propensity in class I PAS-B domains, suggesting a higher level of coupled dynamics between PAS-B domains. Our results highlight how PAS domain intrinsic dynamics are shaped by both their internal architecture and complex-specific interactions, offering new insights into the functional diversification of bHLH-PAS transcription factors.