Following Vaylin's Eternal Empire attack on the Gravestone, both Zakuulan and Alliance forces found themselves prisoners of ARIES on Iokath. To escape from Iokath, they had to battle ARIES' droid army and reclaim their starships. After Theron Shan restored communications, the Alliance forces were able to regroup, utilizing a shuttle remotely piloted from the Gravestone. The Eternal Empire forces suffered substantial losses from the hostile Iokath droids. However, Vaylin managed to locate and rally her troops, enabling them to find and liberate captured Eternal Fleet warships. SCORPIO, an Iokath creation who had previously betrayed both Vaylin and the Alliance, exposed Iokath's history and identified ARIES, the sole self-aware droid, as the greatest danger, capable of eliminating everyone. After ARIES deactivated a planetary shield that had prevented any spacecraft from escaping, SCORPIO and the GEMINI captains discovered the location of ARIES base. The Alliance then launched an assault on the base to confront ARIES, while the Eternal Fleet bombarded the fortress from above. SCORPIO aided the Alliance Commander and Vette in defeating ARIES, and in return, she was allowed to merge her consciousness with Iokath. Shortly thereafter, ARIES' superweapon's capacitors overloaded, engulfing the planet in a wave of lethal radiation. The Gravestone narrowly escaped to hyperspace, as did Vaylin with the majority of the Eternal Fleet, rendering Iokath inaccessible for the foreseeable future.

Iokath, a completely self-sustaining ecosphere that encompassed an entire star, had remained hidden from the rest of the galaxy since the unidentified Iokath species annihilated themselves in a civil war. The only remaining intelligent being on this technological marvel was ARIES, a highly intelligent droid who used other droids as slaves to reshape the world according to his vision. Over three millennia, only a handful of visitors had stumbled upon Iokath, and none had survived to tell the tale. During the war against Zakuul, SCORPIO, herself an Iokath creation with suppressed memories of it, succeeded in unlocking the origins of herself, the Gravestone, and the Eternal Fleet, subsequently bringing all of these vessels to Iokath. The Eternal Fleet was manned by the GEMINI captains and a significant number of Eternal Empire personnel, while the Gravestone carried key members of the Alliance opposing Zakuul and its Eternal Empress, Vaylin. As the ships drew near to and entered Iokath, ARIES activated a superweapon that emitted a blinding light, rendering everyone aboard unconscious. He then strategically positioned them across the surface of Iokath for combat testing, singling out Vaylin and SCORPIO as the most formidable.

One by one, Alliance and Eternal Empire personnel regained consciousness on Iokath's surface, separated from each other. Some received assistance from Iokath remotes, while all faced attacks from various Iokath droids, reprogrammed by ARIES to exhibit hostility towards any foreign presence. ARIES monitored the test results, seeking a worthy successor to control Iokath, appearing as a Human hologram at various technoliths. The Zakuulan forces, although greater in number, suffered significant casualties among both the Knights of Zakuul and Eternal Fleet officers. Meanwhile, Alliance member Theron Shan successfully utilized his cranial cybernetic implant to contact other Alliance members, directing them to a structure known as the Tributary. Along their journey, numerous Alliance members encountered Zakuulan forces, with Koth Vortena encountering an officer seeking surrender before being killed by droids, Kaliyo Djannis achieving twenty-six and a half kills, and Torian Cadera and the Alliance Commander discovering a group of Knights who were all eliminated by the scour swarm droids.

After the Alliance members had all gathered, their position within the Tributary was soon attacked by purifier droids. Theron fired upon the force field console, trapping the droids outside and forcing the Alliance to find an alternative escape route. The Alliance Commander and Vette took the lead to explore, encountering and disabling a colossus droid, with the rest of the Alliance close behind. Theron soon realized that, despite being unable to locate the Gravestone, he could still use his implant to remotely pilot the shuttle left in its hangar. To create a diversion from the droids outside, the team repaired the colossus droid, allowing the Commander to use it against its weaker, yet more numerous, brethren. While the Commander held off the droids in the Tributary Grounds, Theron located his shuttle, remotely piloted it to the Tributary roof, waited for everyone to board, and then took off.

SCORPIO, similarly imprisoned in an unknown location, managed to find a connection node in her cell and gain access to Iokath's vast planetary network. Exploiting ARIES' preoccupation with other prisoners to escape her confinement, SCORPIO employed his own tactic to leave a holographic disguise in her place. By the time ARIES deemed her too dangerous and targeted her with laser fire, she was already far away. Eventually concluding that none of the new arrivals were worthy of inheriting Iokath, ARIES resolved to end the combat simulations. He activated a massive energy shield that would destroy any vessel attempting to leave Iokath and began recharging his superweapon, intending to use it on a lethal setting this time. However, his multiple holo-transmissions enabled SCORPIO to pinpoint his location at ARIES base in Iokath's southern hemisphere and transmit it to the Alliance forces, urging them to stop ARIES before he could destroy them all.

Meanwhile, Empress Vaylin, who awoke alone in her cell, was visited by ARIES, appearing in the hologram of her deceased brother Thexan. Vaylin immediately grew suspicious when she could not sense her brother through the Force and quickly discerned the deception by feeding "Thexan" a falsehood about her past, which he did not correct. Demanding to know the identity of the impersonator, Vaylin used the Force to pull together wall panels into a projectile and hurled it at "Thexan," smashing a wall and revealing a way out of her cell. Vaylin soon encountered the remnants of Eternal Fleet crews and rallied her forces to retake the Fleet from ARIES.

Together, they discovered the control console, from which one of the GEMINI captains released the docked Eternal Fleet warships. However, as the ships prepared to depart, they began colliding with ARIES' energy shield, and Vaylin ordered the source to be found and disabled. A purifier drone landed a lucky shot on Vaylin, who responded by destroying it, rendering the droid harmless. She then took the droid with her to one of the warships, where her loyalists informed her that half of the Eternal Fleet had been recaptured, while the remaining ships could be towed with tractor beams. The GEMINI captain connected to the purifier drone to access its information about ARIES, which revealed that ARIES was about to fire his weapon, which would destroy both organics and the GEMINI droids.

Reaching ARIES base in the shuttle, Theron dropped off the Commander and Vette to confront ARIES, while the rest departed to reclaim the Gravestone, now knowing its location based on the shuttle's last coordinates. They managed to seize the ship right under Vaylin's nose but were pursued by the Eternal Fleet warships. The Commander and Vette stormed the base and attacked ARIES, even as the Eternal Fleet bombarded his base and the superweapon capacitors threatened to overload. Eventually, after ARIES feigned defeat and attempted to betray the Alliance Commander, he was shot in the back and permanently destroyed by SCORPIO. She then lowered the energy shield and urged the Commander to escape before the capacitors on ARIES' superweapon overloaded and engulfed the planet in a wave of lethal radiation.

SCORPIO announced her intention to upload her consciousness into the planetary network, becoming one with Iokath. Since this would prevent her from threatening the Alliance or the galaxy again, the Commander allowed her to proceed, and SCORPIO thanked them before permanently abandoning her droid body. The Commander and Vette rushed outside, where they were picked up by the Gravestone at the last minute. With the planetary shield down, the Eternal Fleet had the opportunity to escape, but Vaylin insisted on eliminating her enemies first and ordered the purifier drone to override the GEMINI captain's programming, restoring it to the default setting. The superweapon then exploded, prompting Vaylin to flee into hyperspace with the majority of the Eternal Fleet, leaving behind several warships to pursue the Gravestone, which itself narrowly escaped to hyperspace with everyone aboard.

The radiation from the exploding superweapon blanketed Iokath, damaging the GEMINI units on the remaining Eternal Fleet warships and causing them to lose contact with their sisters in the GEMINI frequency. Enraged by their failure, Vaylin resolved to have the GEMINI captains obey her without question, as they had before SCORPIO granted them free will. Vaylin brought the purifier drone back to Zakuul and plugged it into the Eternal Throne, from where the droid restored every GEMINI unit to their default setting. Despite the loss of her advisor and some of the Fleet personnel, Vaylin considered regaining full control of the Eternal Fleet a victory, immediately deploying it to attack Alliance outposts and patrols.
Just before the Alliance escaped, SCORPIO transmitted them the schematics for upgrading the Gravestone with Iokath technology. She later sent the Commander one final message, indicating that she was making a home within Iokath's massive planetary network. The Alliance leadership safely returned to Odessen, where the Gravestone was dry-docked to install the new upgrades. Ultimately, Alliance forces regained control of their most powerful weapon without suffering a single casualty, while SCORPIO was out of the picture and unable to threaten the Alliance again. Additionally, the Alliance Commander became aware of a secret phrase that would trigger Vaylin's mental conditioning right before everyone was captured by ARIES, giving the Alliance an edge against the Eternal Empress.
Alliance scouts were dispatched to the Iokath system, but the radiation levels remained dangerously high, disrupting navigation and communications signals and making any exploration impossible. By the time the radiation levels subsided, Empress Vaylin was already dead, and the Alliance had conquered Zakuul, transforming itself into the Eternal Alliance. A clandestine group known as the Order of Zildrog discovered the location of another superweapon known as the Old Gods on Iokath and leaked it to the Eternal Alliance, Galactic Republic, and the Sith Empire. All three parties arrived on Iokath and converged on the superweapon simultaneously, leading to the War on Iokath.
The number of Alliance personnel present may vary depending on player's previous Dark Side choices. During Knights of the Fallen Empire Chapter XIII: Profit and Plunder, the player may have the option to kill or exile either Aric Jorgan or Kaliyo Djannis, depending on choices made during previous Chapter XII: Visions in the Dark. Similarly, during Knights of the Eternal Throne Chapter III: Dark Reunions, the player may have the option to kill Koth Vortena, depending on choices made during Fallen Empire Chapter X: Anarchy in Paradise.
At the end of Chapter V: Ascension, the player can either allow SCORPIO to merge with Iokath as a Light Side choice or kill her for past betrayals moments before she obtains freedom as a Dark Side choice. In the latter case, the Alliance will still obtain schematics for Gravestone upgrades from other information sources collected on Iokath.