For the last thousand years of the Great War, Starscream was in charge of an orbital facility that had the capability of producing Dark Energon, though they maintained only a small stockpile because of its unpredictable and uncontrollable nature. The station's force of neutral soldiers were no match for Megatron's invading forces, while Starscream and Jetfire's repeated warnings that no one could control Dark Energon had no effect on Megatron's determination. Instead, Megatron tempted Starscream with knowledge of his past, reminding him of his demotion from Sky Commander to a mere guard over an all-but-derelict station, and offered to let him join the Decepticons, something Starscream scoffed at — at least, at first. Starscream attempted to destroy the station's stock of Dark Energon before the Decepticon leader could reach it, but failed, and watched, first with amusement as Megatron entered the storage chamber...and then with shock as Megatron infused himself with the substance and bent it to his will within moments. Starscream quickly volunteered his services for the Decepticon cause, causing Jetfire to label him a traitor and leave to warn Zeta Prime. Megatron sent him with Thundercracker and Skywarp to Cybertron to reactivate the Energon Bridge. Starscream performed the mission successfully using his trademark style, flair, and modesty, never mind Megatron's taunting and unreasonable impatience, or Thundercracker's warning him of the danger of certain courses of action, or even Skywarp's cluing in to his constant insults.

During the Battle of Iacon City, Starscream led the Decepticons aerial squadrons and Brawl led the Decepticons' ground assault, while Megatron, Soundwave, and Breakdown went behind enemy lines and tried to secure the Omega Key. When Megatron's group met up with Brawl, Starscream refused to send Dark Energon bombers, saying that he wouldn't let Brawl waste anymore of "his ships". Megatron took issue with Starscream dubbing the bombers his, and overrode Starscream's refusal. Later that evening, while looking for the "real" Omega Key, they ran into it: Omega Supreme. Starscream assumed Megatron was killed when Omega attacked a dropship Megatron was heading for and declared himself Decepticon commander. Shortly afterward, Megatron managed to communicate with Starscream and ordered him to attack Omega Supreme, getting the massive Autobot off Megatron's back. By the time Megatron's group were heading for the Autobot turrets, Starscream was ready to sound a retreat, which Megatron overrode with the threat of marking any retreating Decepticon as "kill on sight". Fortunately, Megatron arrived moments later and managed to defeat Omega Supreme, making the retreat unnecessary. Later on, he was present at the Core of Cybertron as Megatron corrupted it with Dark Energon.

As the Battle of Iacon continued, Starscream fought through Jetfire and Silverbolt, and attacked Optimus's group in the Decagon. However, the Air Commander was injured by Optimus's Energon-axe and forced to retreat. The wound was apparently bad enough to cause him to sit out the remainder of the conflict.

Under Megatron's orders, Starscream and the Combaticons ambushed and captured Optimus Prime under the ruins of Iacon during the assault on the Ark. Starscream's gloating on how he defeated Megatron's nemesis would earn him a blast from the Decepticon's leader's fusion cannon. Starscream's luck would take an uphill turn, however, for Megatron was soon crushed by Metroplex, leaving him the new leader of the Decepticons. At the urging of both Prime and Metroplex, Starscream ordered the Decepticons to retreat.

Starscream's reign as a leader was lackluster at best. He used most of the Decepticon energon and supplies to further his own ego and cover the Decepticon bases with portraits and effigies of himself and constantly broadcasting self glorifying speeches to his troops. Anyone who wasn't on board with Starscream's reign was thrown into the prisons of Kaon. Needless to say, the prisons were full to bursting as barely a handful of Decepticons had any faith in their new leader. When the Autobots acquired the entire energon supply the Decepticons kept in the Sea of Rust. Starscream sent the Combaticons to stop the transport. When the transport was out in the open, Starscream ordered an assault on it, despite the fact the anti-aircraft guns were still functional. As the Decepticons suffered heavy losses, Starscream aborted the mission and ordered a full retreat. The Combaticons ignored the order and brought the transport down, at the cost of half the energon on board. Despite the fact that the Combaticons had saved the mission he had abandoned, Starscream accused them of failing and had them arrested.

Later, Starscream decided to have a coronation for himself (despite the fact he had been in charge for some time now). Though sadly it was not to be, as a newly rebuilt Megatron crashed the event and took his crown back from the would-be king, much to everyone else's elation. Luckily, the Air Commander escaped Megatron's wrath, swearing revenge.

Seeking the means to get back at Megatron, Starscream made his way to Shockwave's lab. He came across Grimlock and promised to free him and his team if they would serve him. The Dinobot kindly refused the offer by throwing him into the control panel, freeing himself. This apparently knocked Starscream out as he didn't get back up. What happened to him afterwords is unknown, since most of Decepticons that might have arrested him were cut to pieces by Grimlock. Fall of Cybertron

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Starscreams primary armament when in his true form consist of three of his favorite weapons. His signature weapon is his Null Ray, which shoots a beam that disables any form of technology it encounters. He also is armed with a Neutron assault rifle, and a Thermo Rocket Cannon. He also carries around EMP Charges, EMP stun Grenades, Explosive charges, and a limited supply of Dark Energon charges. His vehicular jet form is armed with homing rockets and a heavy caliber rapid-fire cannon.

Starscream, like all Cybertronians, can alternate between his humanoid form, and a vehicular form of his choosing. Transforming into an alien jet, he is well known as one of the most dangerous Aces on Cybertron. When in his true form, he can activate jet boosters in his feet, allowing him to fly or hover in the air. They also allow him to boost around the battlefield, dodging attacks that might otherwise hit him. When brute force isn't an option, he often enjoys using his experimental cloaking device. This new technology allows him to become almost invisible, only a slight outline of him is visible in the right conditions. While a powerful tool, this experimental device can only remain active for a short while, and it tends to fail when he activates his weaponry. It also cannot hide his energy signature, nor his voice. This is a problem for Starscream, as he enjoys taunting his opponents.