Histone tails are integral structural and functional components of the eukaryotic nucleosome. These tails, rich in positively charged amino acid residues, interact with the DNA to stabilize the nucleosomal structure. However, capturing the biochemical effects of posttranslational modifications (PTMs) on histone tails in molecular detail using X-ray or NMR techniques remains a challenge due to their intrinsically disordered structure. In this work, we studied the N-terminal portion of the H3 histone protein, a 38-residue tail, that when posttranslationally modified, is implicated in altering the tail’s interaction with the DNA, affecting nucleosomal stability. Using all-atom molecular dynamics simulations for a total of 35 microseconds, we investigated the structure and dynamics of the wildtype H3 tail and seven known nucleosomal PTMs. Based on residues’ contacts with DNA, water, and ions, dihedral angle analysis, and root-mean-square fluctuations of the tail residues, our results show that the H3 tail has a tripartite segmental nature. The three segments, labeled I, II, and III, are separated by the proline residues P16, P30, and P38. A comparison of wildtype H3 tail and proline-to-alanine-mutated H3 tail showed that the prolines function as segmental dividers or hinges of the H3 tail. We show that Segment I is more dynamic than Segments II and III, and Segment I makes multiple transient contacts with the DNA. The PTMs affect the tail’s dynamics to different extents, but the tripartite segmental nature of the tail is preserved. Notably, single-residue modification of the lysine by acetylation or methylations in Segment I versus multiple residue modifications by serine phosphorylation or lysine methylations have marked effects on the tail’s flexibility and interaction with the DNA. This study highlights the significance of proline residues in creating the segmental behavior of the H3 tail.