The receptor-like kinases Brassinosteroid Insensitive 1 (BRI1) and BRI1-Associated Kinase 1 (BAK1) are critical to plant growth and development signaling, serving as co-receptors for brassinosteroid hormones. Possibly because of their importance in these pathways, BRI1 and BAK1 are both highly regulated. Upon brassinosteroid binding, the BRI1 and BAK1 kinase domains (KDs) phosphorylate and activate one another, while among other negative regulatory mechanisms, BAK1 is deactivated in vitro by S-glutathionylation in oxidative conditions. However, the molecular mechanisms of BRI1 and BAK1 regulation and activation remain unclear. In order to investigate the dynamics of fully phosphorylated BRI1 and BAK1 KDs and to understand the mechanism of BAK1 deactivation by S-glutathionylation, we performed extensive all-atom molecular dynamics simulations on the BRI1 and BAK1 core KDs along with BAK1 in all viable singly glutathionylated forms. In non-glutathionylated BRI1 and BAK1, we found considerable disorder in the αC helix, a common regulatory domain in protein kinases (PKs) which must be folded in an active conformation. In order to validate our findings, we performed circular dichroism spectroscopy experiments on the BRI1 αC helix peptide, yielding results consistent with our simulations. Using disorder prediction software on all Arabidopsis thaliana PK sequences, we found that αC helix disorder may be a common feature in plant kinomes. From our simulations of glutathionylated BAK1, we found that S-glutathionylation of Cys408, neighboring the αC helix, destabilized active-like BAK1 conformations, while modification of other Cys residues had little effect. Using Kullback-Leibler divergence, we found that Cys408 S-glutationylation had long-range effects on individual residue conformations. Our results suggest that additional factors beyond phosphorylation are required for BRI1 and BAK1 activation, while supporting an allosteric mechanism of BAK1 deactivation by Cys408 S-glutathionylation. To our knowledge, our simulations represent the first insight into atomistic plant PK dynamics.