This study analyzes regulated dynamics within the MAP kinase, ERK2, following catalytic activation by phosphorylation, using 13C NMR relaxation methods to observe side chain motions of selectively labeled residues (Ile, Leu, Val) on the timescale of μs-ms. ILV 1H-13C methyl-labeled 0P-ERK2 and 2P-ERK2 proteins were prepared, yielding NMR 1H-13C methyl-HMQC spectra with ~100% of the predicted number of peaks. 50% of the peaks, each represents an Ile/Leu/Val methyl side chain, were assigned by site-directed mutagenesis, combined with NMR through-space and through-bond constraints. Twenty percent of assigned methyl side chains showed changes in NMR 13C relaxation dispersion profiles comparing 0P-ERK2 to 2P-ERK2, revealing altered side chain dynamics upon ERK2 phosphorylation. At 25 ºC, Ile, Leu and Val methyl side chains around the catalytic site and MAPK insert of 0P-ERK2 showed rapid exchange (kex = 1,398 ± 105 s-1) that cannot be fit into a well-defined two-site exchange system, whereas no methyl dynamics in the micro- to millisecond time regime were detected in other regions, even upon decreasing temperature to 10 ºC. In contrast, methyl side chain dynamics were observed in broader regions in 2P-ERK2, and each of these side chains in 2P-ERK2 that showed dispersion profile could be fit to a two-site exchange model with well-defined exchange parameters (kex = 354 ± 18 sec-1, population = 17±1%). Thus, in 0P-ERK2, the exchange scenario for Ile, Leu, and Val methyl side chains vary considerably throughout the molecule, whereas in 2P-ERK2, exchange rates that were fast in 0P-ERK2 decrease while exchange rates that were slow in 0P-ERK2 increase, converging to uniform values. We hypothesize that in 2P-ERK2, methyl side chain dynamics may become more concerted than in 0P-ERK2, so that phosphorylation creates a more dynamically coupled system, which might help stabilize the transition state during catalysis.