2256 to 2259
The Agamemnon would be commanded for the next three years by John Sheridan until 2259, when he was named to replace Jeffrey Sinclair as the commander of Babylon 5. The Agamemnon met with a supply vessel about hijackers. 
At that point, Captain James was named as the next commander of the Agamemnon. A few months after Sheridan's transfer the Agamemnon took part in his rescue from the Streib. When the Streib ejected those they kidnapped into space, the Agamemnon destroyed the Streib starship. 
In 2260, the Agamemnon was patrolling the solar system when Sheridan took the White Star to destroy the Shadow cruiser being studied by Earth Alliance forces. The Shadow vessel had been activated when a human was merged with the ship to act as a CPU, but it was done incorrectly, and the ship went insane. The Shadow vessel was lured into Jupiter's atmosphere where it was crushed by the pressure and gravity of Jupiter. The Agamemnon was sent to investigate, and found the White Star in the atmosphere. The crew of the Agamemnon did not realize that Sheridan was in command of the White Star. Agamemnon tried to force Sheridan to surrender, but he was able to escape through establishing a jump point at the edge of Jupiter's atmosphere. President Clark used this incident as an excuse to declare martial law. Clark's actions later provoked Sheridan and a number of others in Earthforce to go to war against Clark.
The Earth Civil War
During the Earth civil war to overthrow President Clark the Agamemnon defected to rebel forces led by Sheridan. She participated in a number of actions against loyalist forces. It was the Agamemnon that retrieved an escape pod from a loyalist ship. This escape pod had a duty officer who knew Clark was planning to ambush Sheridan's forces at Sector 300. Commander Ivanova was able to intercept Clark's Shadow enhanced starships, and even though Ivanova was critically injured she was able to destroy all the Shadow enhanced ships.
Ivanova asked Sheridan to command the final battle from the Agamemnon to give a legitimate appearance to Sheridan's forces. Sheridan and Captain James agreed to this. Sheridan arranged for telepaths altered by the Shadows for use as CPUs in their ships to be snuck on board the loyalist ships at Mars. This disabled nearly all the forces, and the White Stars disabled the remaining ships. Even though it cost the 30 telepaths their lives, it saved the crews of these ships - nearly 30,000 men and women.
When the Agamemnon and the rest of Sheridan's fleet arrived at Earth, the Senate rose up and went to arrest Clark. President Clark knew he was going to be arrested, so in a final vindictive act he turned Earth's planetary defense grid on the planet as a Scorched Earth policy and committed suicide. Sheridan's forces destroyed the defense grid. The last platform was destroyed by the EAS Apollo, under the command of General Leftcourt - the commander of the loyalist forces. During this final battle, the Agamemnon was seriously damaged by the defense platforms, and its weapons were disabled. In a desperate attempt to destroy the last defense platform before it could fire on North America's eastern seaboard, Sheridan ordered the Agamemnon to ram it. Lefcourt's last minute intervention saved not only the crew of the Agamemnon but millions of people living on Earth.
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