The recent outbreak of the severe acute respiratory syndrome virus 2 (SARS-CoV-2), the causative agent of an ongoing global pandemic, has led to an unprecedented effort in vaccine and therapeutics development. The persistent emergence of SARS-CoV-2 escape variants capable of evading immune responses and therapeutic monoclonal antibodies (mAbs) highlights the need to identify conserved, immunogenic epitopes that can provide broad protection against coronaviruses. Currently, seven coronaviruses across two genera account for the majority of human infections, namely alphacoronaviruses NL63 and 229E, and betacoronaviruses SARS-CoV-2, severe acute respiratory syndrome virus (SARS-CoV), Middle East respiratory syndrome virus (MERS-CoV), OC43, and HKU 1. Since the coronavirus spike protein is essential for viral attachment and fusion with the host cell, and is the major target of neutralizing antibodies, in this study our goal was to identify mAbs that are crossreactive to multiple coronavirus spike proteins. Using a broad screening and an improved isolation approach, we isolated seven mAbs that bind to the spike protein of all seven human-infecting coronaviruses. These mAbs were isolated from SARS-CoV-2 immune donors, target the highly conserved fusion peptide epitope essential for viral fusion, and acquire affinity and breath through somatic mutations. Despite targeting a conserved epitope, only some mAbs displayed broad in vitro neutralizing capacity against alpha and betacoronaviruses, including animal WIV-1 and PDF-2180. Two selected antibodies also neutralize Omicron BA.1 and BA.2 live viruses and reduce viral burden and lung pathology in vivo. Structural and functional analyses showed that the fusion peptide–specific mAbs bound with different modalities to a cryptic epitope hidden in prefusion-stabilized SARS-CoV-2 spike protein, which became exposed upon binding of angiotensin-converting enzyme 2 (ACE2) or ACE2-mimicking mAbs. Alphacoronaviruses, on the other hand, readily expose the fusion peptide region, suggesting that genus-specific structural differences might affect the accessibility of this immunogenic site. Structure and sequence analysis revealed that the fusion peptide flanking regions, which were suggested to play a role in conformational changes of spike protein, are conserved in alphacoronaviruses and contribute to the accessibility of the fusion peptide. Indeed, SARS-CoV-2 spike engineered to harbor a substituted fusion peptide-flanking region from alphacoronaviruses displayed enhanced accessibility of the fusion peptide to anti-fusion peptide mAbs. In combination with the 2P prefusion-stabilizing mutations that would otherwise lock the spike protein in a prefusion conformational state, this engineered spike chimera had improved bindings to broadly reactive anti fusion peptide and anti-stem helix antibodies by several folds while maintaining the ability to bind to anti-RBD antibodies. Altogether, these data indicate that the engineered SARS-CoV-2 spike chimera protein may lead to a better elicitation of broadly-neutralizing anti-fusion peptide mAbs than the current 2P-stabilized mRNA vaccines and present a rational design of next generation universal coronavirus vaccines.