AbstractAllosteric mechanisms provide finely‐tuned control over signalling proteins. Proteins of the same family may share high sequence identity and structural similarity but show distinct traits of allosteric control and evolutionary divergent regulation. Revealing the determinants of such properties may be important to understand the molecular bases of different regulatory pathways. Herein, we investigate whether and how evolutionarily‐divergent traits of allosteric regulation in homologous proteins can be decoded in terms of internal dynamics and interaction networks that support functionally oriented conformations. In this framework, we start from the comparative analysis of the dynamics and energetics of the yeast MAP Kinases (MAPKs) Fus3 and Kss1 in their native basins. Importantly, distinctive dynamic and energetic stabilization features emerge, which can be related to the two proteins’ differential ability to be phosphorylated and engage with the allosteric activator Ste5. We then expanded our study to other evolutionarily‐related MAPKs. We show that the dynamical and energetical traits defining the distinct regulatory profiles of Fus3 and Kss1 can be traced along their evolutionary tree. Overall, our approach is able to reconnect (latent) allostery with the principal elements of protein structural stabilization and dynamics, showing how allosteric regulation was encrypted in MAPKs structure well before Ste5 appearance.