Allostery constitutes the major mechanism of intra- and interprotein signaling. Detecting these signaling channels, their underlying structural rearrangements and especially transition dynamics is challenging, as it requires a detailed analysis down to atomic scales and timescales that cover several orders of magnitude. We here present an integrative research approach to detect and follow allosteric information transfer across multiple time- and length scales. We employ molecular dynamics simulations on a multi-μs scale combined with nanosecond fluorescence correlation spectroscopy and neutron scattering experiments, including neutron spin echo experiments, to verify the predicted dynamics and structural changes. Using the heat shock protein 90 (Hsp90) as the test system, we reveal molecule-spanning and highly diffusive dynamics on the order of 100 ns that may serve as the dynamic basis for allosteric changes. Furthermore, we can follow protein dynamics upon hydrolysis of ATP to ADP from Angstroms and nanoseconds (bond ruptures and local rearrangements) to nanometers and microseconds (protein domain reorientations). Intriguingly, a single amino acid is crucial for transferring structural information from the nucleotide binding site to the full protein dimer.