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The Cruiser is larger than the Covenant Light Cruiser but is smaller than the Covenant Carrier. They are armed with five Plasma Turrets and laterally-mounted pulse lasers, but lack a compliment of supplementary Seraph Starfighters. Like other Covenant ships, the Covenant Cruiser is roughly oblong in shape with touches of a purple and blue color scheme.
- The Rapid Conversion, the Covenant vessel that partook in the First Battle of Harvest, was a Covenant Cruiser.
- Six Covenant Cruisers accompanied the Covenant Flagship Ascendant Justice on a reconnaissance mission to the ruins of Alpha Halo after its destruction by UNSC forces. One cruiser had one of its five plasma turrets destroyed by John-117 operating a C709 Longsword starfighter. After the Master Chief and a group of UNSC ground forces were able to hijack the Flagship, one Cruiser jumped to Slipspace to alert Covenant forces of the destruction of Alpha Halo and UNSC activity in the area.
- An Unnamed Covenant Cruiser was one of many Covenant Cruisers involved in the Battle of Reach. The Unnamed Cruiser was destroyed by Joshua-029, Kelly-087 and Frederic-104.