Background: Venoms from ant (Formicidae) are chemically extraordinarily diverse, yet their genomic architecture and evolutionary dynamics remain opaque. The "aculeatoxin hypothesis" assumes that most venom peptides in stinging insects (aculeate) evolutionarily derive from a single gene family, the aculeatoxins. The recent refutation of this hypothesis for bees raises fundamental questions about venom evolution in ants, which contribute most aculeatoxins. Methods: In order to trace venom peptide evolution, we performed synteny-aware comparative genomics across 25 ant species spanning major subfamilies. We analyzed phylogeny through sequences, structures, and embeddings from protein Language Model (pLMs). Results: We identified three conserved genomic regions (GR1-GR3) as evolutionary hotspots for ant venom genes, each exhibiting distinct evolutionary dynamics. Most remarkably, we discovered genuine melittin orthologs in ants at the conserved bee syntenic position (GR2), pushing the origin of this scaffold back to early aculeates, with a possible origin deeper in Hymenoptera. Gene copy numbers vary dramatically (0-17 genes per region), with predatory species showing expansions and formicine ants (subfamily Formicinae, which rely on formic acid spraying) showing reductions. Twenty-two distinct toxin clades emerge, with region-specific distributions suggesting repeated recruitment to conserved platforms. Significance: Ants evolutionarily succeed by combining single-copy conservation (bee-like at GR2), massive gene duplication (snake-like at GR1), and repeated lineage-specific recruitment to conserved genomic platforms (GR3). This multi-modal evolution on stable genomic scaffolds, evidenced here, reconciles previously conflicting models of venom evolution and reveals how gen