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The Mec1/ATR kinase is crucial for genome stability, yet the mechanism by which it prevents gross chromosomal rearrangements (GCRs) remains unknown. Here we find that in cells with deficient Mec1 signaling, GCRs accumulate due to the deregulation of multiple steps in homologous recombination (HR). Mec1 primarily suppresses GCRs through its role in activating the canonical checkpoint kinase Rad53, which ensures the proper control of DNA end resection. Upon loss of Rad53 signaling and resection control, Mec1 becomes hyperactivated and triggers a salvage pathway in which the Sgs1 helicase is recruited to sites of DNA lesions via the 911-Dpb11 scaffolds and phosphorylated by Mec1 to favor heteroduplex rejection and limit HR-driven GCR accumulation. Fusing an ssDNA recognition domain to Sgs1 bypasses the requirement of Mec1 signaling for GCR suppression and nearly eliminates D-loop formation, thus preventing non-allelic recombination events. We propose that Mec1 regulates multiple steps of HR to prevent GCRs while ensuring balanced HR usage when needed for promoting tolerance to replication stress. Synopsis: Chromosomal rearrangements (GCR) are a hallmark of many cancers, but how cells prevent these deleterious events remains incompletely understood. This work analyzes how the DNA-damage signaling kinase Mec1/ATR suppresses chromosomal rearrangements, uncovering an intricate interplay between the checkpoint and the Sgs1 helicase. In yeast cells lacking downstream DNA damage checkpoint signaling, Mec1 is hyperactivated and targets the Sgs1 helicase. Recruitment of Sgs1 helicase and its phosphorylation by Mec1 are crucial for GCR suppression in cells lacking downstream DNA damage checkpoint signaling. Engineered Sgs1 recruitment suppresses GCRs and reduces D-loop levels in cells defective for Mec1 signaling. Phosphorylation of Sgs1 by Mec1 regulates its ability to reject recombination between homeologous sequences. Phosphorylation of Sgs1 by Mec1 regulates its ability to reject recombination between homeologous sequences, showing an intricate interplay between the yeast DNA damage checkpoint and the Sgs1 helicase. [ABSTRACT FROM AUTHOR]