The continued risk of zoonotic coronavirus spillover, highlighted by the emergence of SARS-CoV-2, underscores the need to define conserved and structurally accessible regions of the Spike glycoprotein that can support broad antiviral strategies. While most antibody studies concentrate on the variable S1 subunit, the fusion machinery within S2 contains more conserved helices and heptad-repeat elements that represent promising, but comparatively undercharacterized, targets. We isolated monoclonal antibodies from COVID-19 convalescent donors that recognize two conserved S2 epitopes: the central helix (CH) and a membrane-proximal region in heptad repeat 2 (HR2), which we designate the lower stalk (LS). CH-directed antibodies showed broad cross-reactivity across betacoronaviruses, whereas LS-directed antibodies were largely restricted to sarbecoviruses. To define the structural basis of this reactivity, we determined sub-4 Å cryo-EM structures of three CH antibodies—ch.005, ch.007, and ch.010—bound to prefusion-stabilized SARS-CoV-2 S2, revealing distinct binding orientations and contact residues relative to previously described CH antibodies. In parallel, a sub-2 Å X-ray crystal structure of the ls.019 Fab bound to an LS peptide provides high-resolution insight into antibody recognition of this membrane-proximal epitope. Together, these findings clarify how human antibodies engage conserved elements of the coronavirus fusion machinery and highlight the central helix and lower stalk as structurally vulnerable sites that may inform the design of broad-spectrum antibody therapeutics and vaccines.