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This flotilla was composed of multiple fleets of war, including the Second Fleet of Homogeneous Clarity. During the conclusion of initial conflict between the UNSC and the Covenant in 2552, this fleet was decimated due to the start of the Great Schism, which divided the vessels by race of captaincy as the Sangheili and the Jiralhanae went to war, and by the appearance of the Flood.
Following the former event, many of the ships in the defense fleet engaged one another in combat around the infested remains of High Charity, with the greater Covenant leadership either dead or otherwise unable to intervene. The Loyalist vessels, captained by Jiralhanae, fled to Earth to aid the Prophet of Truth, while the Separatist vessels, captained by Sangheili, remaining with the holy city in an attempt to prevent the Flood onboard from spreading. When a single Flood-infected CCS-class ship broke the quarantine and crashed on Earth, several Separatist craft from the former defense fleet pursued it.
Despite the efforts of the Sangheili, High Charity itself broke through the cordon of former defense ships and entered the Portal at Earth. It is unknown what became of the surviving elements of this fleet on both sides of the civil war following the conclusion of the Human-Covenant conflict. The fleet itself was disbanded with the conclusion of the Covenant as a galactic political entity.