The struggle known as the War on Iokath involved the Eternal Alliance, the Sith Empire after its re-establishment, and the Galactic Republic, all vying for dominance over the artificial planet Iokath and its valuable resources. This conflict was masterminded by the enigmatic Order of Zildrog, who provided all three factions with identical information about a potent superweapon. Consequently, these factions converged at the same location simultaneously, each aiming to seize control. Jace Malcom, the Supreme Commander of the Republic, and Darth Acina, the Sith Empress, dispatched representatives to negotiate with the Alliance Commander. The Commander chose to support the Republic against the Empire, leading to open warfare. During the conflict, the Alliance's adversaries managed to reverse-engineer access to the superweapon and prepared to activate it, oblivious to the peril it held. The Commander and Theron Shan hurried to intervene, but they were too late to prevent Empress Acina from awakening Tyth, the God of Rage. Acina subsequently lost control of the throne and was killed by a power surge. The Alliance Commander was then lured into a trap by a member of the Order, but they managed to command the Eternal Fleet to attack Tyth, incapacitating him and allowing the Alliance time to confront the other machine gods. Despite the significant blow to the Empire, the importance of Iokath's resources led them to persist in the battle for months, ultimately resulting in a stalemate for all involved.
Iokath, a colossal, self-sustaining ecosphere that completely surrounded its star, had remained hidden from the rest of the galaxy since the Iokath species annihilated itself in a civil war. More than three millennia later, the Alliance that fought a war against Zakuul rediscovered it. However, during the initial exploration, an ancient superweapon detonated, engulfing the entire planet in a wave of lethal radiation. This disrupted navigation and communication signals, rendering further exploration impossible. The Alliance was compelled to abandon the planet temporarily, though they stationed scouts in the system to monitor radiation levels, forced to await their decline. By the time radiation levels were safe for organics, the Alliance had already triumphed over the Eternal Empire of Zakuul and gained control of its Eternal Fleet, itself a creation of Iokath.
In an attempt to infiltrate the Order of Zildrog, Theron Shan plotted to ensnare the Alliance Commander to demonstrate his commitment to the Order's goals. Acting independently, he simultaneously leaked the location of another Iokath superweapon, known as the Six Gods, to the Eternal Alliance, the Sith Empire, and the Galactic Republic. All three factions expressed interest in the anonymous data and dispatched teams to secure the superweapon, led by Lana Beniko, head of Alliance Intelligence, Jace Malcom, Supreme Commander of the Republic Military, and Darth Acina, the Sith Empress, respectively.
Beniko, who located the superweapon first, contacted the Alliance base on Odessen to deliver a status report. However, she was interrupted by the arrival of Republic and Imperial forces at the same coordinates. Soldiers from these two sides engaged each other, while Beniko and her team evaded detection and retreated to the Fleet Spire, where they established a stronghold. Upon learning of this development, the Commander summoned the entire Eternal Fleet to Iokath, while personally traveling there with Theron Shan. Both sides sent emissaries to the Fleet Spire to negotiate with the Alliance: Captain Elara Dorne of the Republic Army and Major Malavai Quinn of the Imperial Army, respectively. However, suspecting them of being assassins, Beniko ordered their capture.
By the time Alliance forces emerged from hyperspace, the Imperial and Republic fleets were already in orbit around Iokath, but had not yet engaged in combat. At this point, a signal from the planet's surface severed the connection between the Eternal Throne and the Eternal Fleet warships, rendering the Eternal Fleet dormant. The Commander and Shan proceeded to the surface in a Zakuulan starfighter and reunited with Beniko at the Fleet Spire. Her captives requested an audience with their superiors, leading to a three-way holoconference between the leaders of the present governments. Both Supreme Commander Malcom and Empress Acina asserted their claim to the superweapon and formally requested the Alliance to join their side in the ongoing conflict. The Commander consulted their advisors. Beniko suggested supporting the Sith Empire, while Shan argued that the Republic was a more dependable ally. However, both pledged to support their Commander regardless of their decision.
The Commander ultimately chose to ally with the Republic, prompting the Empire to immediately launch a retaliatory strike when Major Quinn detonated a flash grenade and escaped amidst the chaos. Simultaneously, the fleets in orbit engaged each other. The Commander instructed Beniko to hold the Fleet Spire, while they and Theron Shan traveled to Malcolm's base to assist in repelling the Imperial assault. Subsequently, the two met with the Supreme Commander and concluded that they needed an advantage to overcome the opposing side's base defenses. Informed about a nearby Iokath weapons cache, the Commander and Shan ventured there to acquire Iokath weapons and knowledge of their use. Inside, Shan accessed files on an ancient console, discovering that the superweapon they were fighting over was powerful enough to obliterate all organic life on Iokath in the distant past, as well as ten trillion lives on other planets.
Meanwhile, the Imperials utilized the schematics they had obtained to engineer backdoor access into the superweapon and modified an Iokath throne to serve as an interface. When the Commander and Shan returned to the Republic base with the weapons, Acina contacted them via holocall, boasting of having access to the superweapon. She asserted that their victory was inevitable and refused to heed warnings about the danger it posed. To prevent them from activating the superweapon, the Commander and Shan boarded a walker enhanced with Iokath weaponry and used it to storm Acina's base. They reached the modified throne, but were too late to stop the Empress from assuming and activating it. This triggered a powerful power surge that awakened the Six Gods and mortally wounded Acina, who soon succumbed to her injuries. The power surge also deactivated the signal that had kept the Eternal Fleet in lockdown, bringing it back online.
To prevent the superweapon from spiraling out of control, the Commander ordered the Eternal Fleet to charge the turbolaser batteries and rushed to the superweapon control center, while Shan remained behind to delay its full activation. Inside the complex, the Commander occupied another throne and encountered Tyth, the first of the Six Gods to reawaken. Tyth revealed to the mortal that a traitor within their ranks had lured them to Iokath, just as a member of the Order of Zildrog sabotaged the throne the Commander was on. Tyth unleashed an energy beam that destroyed an Eternal Fleet warship, but the Commander managed to endure the pain and ordered the rest of the Fleet to fire on the giant droid, incapacitating it and forcing it to retreat.
The Commander's body was transported back to the Fleet Spire for recovery. Upon regaining consciousness, they were informed by Malcolm that, despite the loss of their Empress, the Empire refused to surrender and continued to wage war for control of Iokath. Meanwhile, Tyth was preparing for a counterattack, and the other machine gods were poised to join him. Determined to secure complete control over Iokath's resources, the Alliance continued to fight for control of its surface. The Commander met with the Scions of Zakuul, who traveled to Iokath to assist them in fulfilling their destiny. The Scion leader Oramis informed the Commander about the significance of the Six Gods to Zakuul's history, explaining the grave danger they posed. The Alliance forces eventually confronted the Six Gods directly, destroying them before they could wreak havoc on the galaxy once again. Despite the Alliance's support, the war between the Republic and the Empire eventually devolved into a stalemate. However, after recovering a large shipment of adegan crystals from Umbara, Lana Beniko expressed confidence that their power would enable them to secure victory. Following Acina's death, Darth Vowrawn declared himself the new Emperor of the Sith and ordered a cessation of all operations on Iokath while he consolidated his power.
The events on Iokath can unfold in two drastically different ways, depending on the player's choice to support either the Republic or the Sith Empire, which will have significant consequences in subsequent story updates. Neither choice represents a light or a dark side option, and players can choose to side against their original faction, making both choices equally valid. Despite this, players who side with a different faction will remain unable to travel to the other side's fleet and capital worlds or participate in activities with players on that side outside of Iokath. While the original choice remains locked from a story standpoint, players can change their nominal allegiance daily, allowing them to complete repeatable missions on both sides.
Siding with either the Empire or the Republic also grants the player Malavai Quinn or Elara Dorne, respectively, as a companion. However, the other can still be reclaimed from a terminal on Odessen for use in non-storyline purposes. Players of the Trooper and Warrior classes also receive additional lines and cutscenes with their returning companions. During these scenes, Dorne can refuse to rejoin Meteor if the player made specific dark side choices during Knights of the Fallen Empire and Knights of the Eternal Throne, while Quinn will attempt to return to his master even if Empire's Wrath sided with the Republic, giving players a dark side option to kill him for his past betrayal.
If the player sides with the Republic, Malcom will approve of this decision, while Acina will mock them and instruct Quinn to proceed with his orders, leading to his distraction and escape. Acina will then request the Commander's psychological profile from Quinn, after which she will personally travel to the surface of Iokath. Meanwhile, Malcom will encounter his son, Theron Shan, and the two will reconcile. Faced with Acina's threat to use the superweapon, Malcom will present the Commander with the walker Nova Strider, enabling them to reach Acina just as she activates her throne. The throne will reject Acina's input and kill her, prompting Theron to remark that he respected her as much as he could respect a Sith, while Quinn escapes again in the confusion.
Following Acina's death, Darth Vowrawn will declare himself the new Emperor and order a halt to all progress on Iokath while he consolidates his power. Imperials will fight against the Alliance with renewed fervor, seeking to avenge the beloved Empress, and will collaborate with the Umbarans on the adegan crystals.
If the player sides with the Empire, Malcom will dismiss them and signal Dorne, who also escapes and reports the Alliance leader's psychological profile to the Supreme Commander. Meanwhile, the Commander will meet with Acina, who is delighted at the prospect of spilling Republic blood once more. Theron will have no choice but to advise his superiors on how to defeat his father, who will disown him during his ultimatum call to the Empire. Acina will give the Commander the walker Crimson Talon, urging them to crush their Republic enemies. Facing his father about to claim the throne, Theron will shoot him, but fail to prevent the throne's activation. Malcom then loses control of the throne, prompting Dorne to flee, while Theron rushes to his father's side. Saying that he is sorry for his actions and asking to tell Satele Shan the same, Malcom will die in his son's arms, causing him serious grief.
Theron will try to maintain a cool exterior, but will be seriously hurt inside, and will make several donations to charities in his father's name, trying to deal with his grief. The death of the Supreme Commander will also lead to the resignation of Supreme Chancellor Jebevel Madon, with Galena Rans appointed as the interim Chancellor, while the Republic faces political stagnation due to the complicated nature of the elections for a proper successor.