When Optimus Prime removed the Plasma Energy Chamber poisoning Cybertron's core with Dark Energon, it informed him that while healing, the planet could not sustain a fraction of the life it currently did, and the Autobots needed to leave. Optimus announced Project Generation One to his comrades, many of whom deemed the notion suicidal as the Cybertronians had not left the planet since the Golden Age. Regardless, Jazz said he would rather die on a starship than on a planet, and declared "Let's build this Ark."
Alpha Trion oversaw the Ark's construction in the Well of All Sparks, installing Teletraan-1 inside, while Optimus drew out and crashed Trypticon aboard the Eight Track. When they returned, the Ark was completed and they boarded the ship. Sideswipe was appointed the pilot. Alpha Trion refused a place, aware Vector Sigma would keep him alive, while Omega Supreme, Jetfire, Ultra Magnus, Springer and the Wreckers sacrificed a chance to leave, giving time for the Ark to launch by keeping Trypticon at bay.
However, Trypticon transformed into the Nemesis and pursued the Ark into the last space bridge, but when it emerged, the Decepticons were nowhere to be found. The Ark was outside an unknown spiral galaxy where the AllSpark was detected. Bumblebee asked Optimus if they knew the way home: he replied the Matrix of Leadership would guide them back one day. Exodus
The Ark emerged from the defunct Spacebridge without any major visible casualties. Its archives were checked for any maps or direction its passengers might use, until it was discovered that they had neared a long lost colony of Cybertronians on a planet known as Velocitron. The Ark was later brought onto the surface of the speed-centred planet and was being repaired until an explosion that took place a certain distance from its hull led Optimus Prime to believe that the Ark's age — it being described as an 'ancient machine' — and its suffering of a Spacebridge malfunction might have been the cause of some internal failure that led to the explosion. He was later informed by Silverbolt that the explosion was the result of sabotage and Optimus suspected they had a traitor on board. Much later when the Ark was parked low in Junkion's orbit and Optimus was coming to terms with the Junkion leader Wreck-Gar, the ship suddenly plummeted toward the surface of the junk planetoid, embedding itself in the ground, and causing a ripple of shock to sweep over the planet. Later Optimus was told by Velocitronian passengers Clocker and Mainspring that they had checked the Ark over before the incident, and they had done so with focus on the ship's fuel reservoir, and that everything had been safe, save for the tiny rupture in it. That they said was not enough to cause the Ark's fall. Once again the accident was revealed to be the result of sabotage, thus deepening Optimus' suspicion of a traitor in their midst. Still later when Junkion was falling apart as a result of the extraction of the Requiem Blaster from the planetoid's core, the Ark had to take off minus some of its intended repairs, with additional damage taken from the seekers Starscream, Thundercracker, and Slipstream's missiles. It was then ordered to turn back toward the remains of Junkion as part of a newly fabricated plan that Optimus engineered in order to play upon Megatron's desire to kill and so contain the Decepticon threat for a while. As it was doing so it had some trouble resisting the gravitational pull of the Requiem Blaster grafted onto the Nemesis. When Megatron discovered the direction in which the AllSpark was to be found, the Ark was made to pursue the Nemesis, without two of its passengers, Clocker and Mainspring, who left with the other components of Nexus Prime. The Ark also had the Star Seekers' ship, the Tidal Wave, in pursuit of it.
- The Ark never made an appearance in Transformers Prime, though it was mentioned by Arcee to Jack. She says there were other Autobots out there who escaped in the Ark, who are now 'scattered to the winds'.