Potassium channels are membrane proteins critical for electrochemical regulation and function in almost all animal cells. In humans, many diseases are associated with mutations in potassium channels, including life-threatening arrhythmias such as Long-QT Syndrome. The process of potassium channel folding and oligomerization is disrupted in many genetic misfolding diseases but remains poorly understood. Outstanding questions concern the structure of folding intermediates, the sequential events involving selectivity filter folding and pore helix insertion to produce the native tetramer, thermodynamic characterization, and the role and generalizability of a protein-dense phase. We have extensively studied the in vitro folding behavior of KcsA, a robust model system for ion channel folding for many human potassium channels such as hERG and Kv1.2. Here we characterize a novel tetrameric species under thermal denaturation with circular dichroism, tryptophan fluorescence, and SDS-PAGE. This state consists of a non-native bundle of transmembrane helices with displaced and dynamic pore helices, which we demonstrate to be metastable using our Upside force field. We also present results from hydrogen-deuterium exchange mass spectrometry (HDX-MS) that demonstrate the extensive stabilization of the KcsA tetramer compared to the monomer. Most notably, we adapted HDX pulse-labeling to membrane protein folding in liposomes to observe site-resolved changes in hydrogen bond formation and stability during oligomerization for the first time. We observe rapid formation of secondary structure in the transmembrane glycine zipper and the inner half of the pore helix, followed by slower folding of the selectivity filter, turret, and outer half of the pore helix on the same slow timescales of tetramer formation. In the context of our previous work, this suggests that these slow-folding structures act as an architectural "keystone" that is assembled last to stabilize the structure into its native fold.