Triumphant

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The Star Fox team's mothership, Great Fox II, arrives at an underground base on the icy planet of Fichina, for maintenance, resupply and rest for its crew. Struggling to find meaning in their exploration, Captain Fox McCloud reveals that he no longer wishes to be part of the team and will be leaving soon; he recommends Peppy as his replacement, but his teammates encourage him to stay. Later, Slippy is reunited with his father Beltino, and the two reconcile. Slippy encourages Falco to do the same with his father, Chester, and the two reconcile over the phone as Slippy sits right next to Falco to boost his confidence. Fox and Peppy work to keep the mothership operational. Peppy reminds Fox that he's turning 24 the following day, but Fox doesn't wish to celebrate his birthday because that was the day his parents passed away. Peppy reiterates that it wasn't his fault that his parents died and convinces him to celebrate his birthday for one.

The following day, Peppy, Falco, Slippy, Bill, Beltino, and Katt make a surprise birthday party for Fox. Before Fox can blow the candles on his birthday cake, Star Fox receives an urgent message from General Pepper. Great Fox is dispatched on a rescue mission after an escape pod drifts out of the Sector β (beta) nebula. Its occupant, Thaddeus, explains that he and his small crew were exploring the galaxy in his ship in search of a new homeworld with food and resources. They've been wandering space ever since Mercurial, their homeworld, located in the now-extinct Aggerian System, was invaded by Aparoids, a race of insect-like creatures that are part-machine, part-life form. They have the ability to control other technology and lifeforms in a viral manner called Aparoidedation.

In a flashback, the Aparoids assimilated with planet Mercurial and turned it into an Aparoid hatchery. The Aparoids also assimilated with most of the Mercurians, making them members of the Aparoid race and totally obedient to the Aparoid Queen. Thaddeus and a small number of survivors managed to escape Mercurial on an old and extremely unstable mothership that belonged to Thaddeus' great grandfather, a space explorer. While Thaddeus and his crew explored the galaxy, their ship malfunctioned and crash-landed on Sauria, a planet inhabited by multiple tribes of many dinosaurs, located in the Sector β (beta) nebula, in the Lylat System. His crew was captured by members of a militaristic band of reptilian pirates known as the SharpClaw Tribe, who serve General Scales, a ruthless dictator geared towards taking control of Sauria. Before the SharpClaw could capture him, Thaddeus fled the planet on an escape pod, the last one from his mothership.

The escape pod was programmed to land in Fichina, which was the "nearest" planet, but it suddenly stopped working, meaning that the escape pod was floating in space with no destination. Thaddeus begged Star Fox to rescue him and help him save his crew, which are currently being held hostage by the SharpClaw in Sauria. Fox asked for some compensation in return, but Peppy scolded him for his lack of empathy and sensitivity, making him feel guilty and convincing him of making an exception and taking the mission without asking anything in return. Star Fox rescues Thaddeus and heads towards Sauria. They come across Meteo, also known as the Asteroid Belt, a dense field of planetoids located in the Lylat system between Fichina and Sector β (beta). The asteroids tear the Great Fox apart. The crew abandons the Great Fox on escape pods before it crashes on Sauria. The crash results in a massive explosion and the crew get divided and lands in different parts of the planet, really far away from each other. Fox searches for the others and is surprised by a sudden earthquake. The planet of Sauria had begun to crack itself apart. Fox comes across the King and Queen of the EarthWalker Tribe, who tell him that General Scales stole four Spellstones from the planet's two Force Point Temples, which is why the planet is tearing apart. The SpellStones were created by the Krazoa Spirits of Sauria, filled with dark matter that absorbs the energy of the planet and holds it together.

Resolving to prevent the planet from breaking up further and restore it to its original unity, Fox traverses the planet in search of the stones, with the help of the King's and Queen's son, Prince Tricky. After wandering the jungle for hours, Peppy and Falco encounter each other and begin to search for the others, but they are pursued and apprehended by soldiers of the SharpClaw. They are brought to the dungeons of the Krazoa Palace, where Thaddeus and his crew are also being held, hostage.

Elsewhere on the planet, Slippy is pursued by a three-headed dragon. Krystal, a scavenger who previously escaped Scales' encampment where her parents were killed, has an intense duel with the beast using her magical staff. She manages to kill off the beast and saves Slippy. After he mentions that he was a freelance mechanic/engineer during his academy days who fixed several spacecraft and weapons designed by Space Dynamics Ltd., Krystal takes him to her makeshift home, the grounded Voyager-27, an early vessel manufactured by Space Dynamics Ltd. for the Cornerian Army which was reported missing over two centuries ago. She reveals that she can use her staff to help Slippy locate his friends, but only if he fixes her "house" so that she can leave Sauria once and for all. Slippy agrees, and he begins to fix the Voyager.

Krystal explains that she was originally native to the planet Cerinia, a planet outside of the Lylat System. In a flashback, she became proficient in using a powerful staff weapon with magical properties that were given to her by a mysterious wizard who told her that she and her staff had a purpose that was yet to be completed. She also became proficient in using her natural abilities of telepathic reading and perception. Her brother was the one who found the Voyager-27 in an abandoned salvage yard. The two worked together to restore it. One day, Cerinia was invaded by the Aparoids, who turned it into a hatchery. Krystal managed to save her parents, but she couldn't save her brother, who was converted into a member of the Aparoid race. Krystal fled Cerinia with her parents on the Voyager-27. An Aparoid knocked the ship out of alignment and began flaring her psychic senses with lots of activity, giving her an unbearable headache. Her headache prevented her from correcting the trajectory in time and the ship tore off at faster than light speed. The ship ended its trajectory in Sauria, where it had a gruff landing. Krystal and her parents excited the Voyager-27 and were captured by the SharpClaw while they explored the planet. They were brought to General Scales, who killed Krystal's parents in her presence. Krystal fought Scales and his soldiers with her staff and managed to escape, taking refuge on the Voyager-27.

Fox and Tricky return the SpellStones to their temples, reunite with Slippy, and meet Krystal. Tricky explains that while the planet did stop cracking apart as a result of the SpellStones being placed within the temples, the pieces of the planet couldn't return to the main body without the six Krazoa Spirits, which are peace spirits and bringers of life to Sauria, who also make flow the magic of the Spellstones. Tricky reveals that General Scales took one of the six Krazoa Spirits. The remaining five were hidden from Scales around Sauria by the EarthWalkers. Krystal agrees to join Fox, Tricky and Slippy in their search for the Krazoa Spirits. Tricky guides them to the Krazoa Spirits and the four manage to retrieve five of the six Krazoa Spirits.

They go to the Krazoa Palace, restore the five spirits and rescue Peppy, Falco, Thaddeus, and his crew. Krystal has a brief fight with Scales, who attempted to kill her using his supernatural abilities while she defended herself with her staff, although she was unable to kill him. She uses her staff to retrieve the last Krazoa Spirit, which was residing inside of General Scales, making him immortal and giving him supernatural abilities. With the last Krazoa Spirit restored, the pieces of the planet returned to the main body. Krystal and Scales have a final confrontation, which ends with Scales' death on the hands of Krystal and her staff. Feeling guilty for being responsible for a murder, and afraid of what the power of her staff might do to her, she destroys it and gets rid of it, believing that she had completed the purpose that the mysterious wizard told her many years ago when he gave it to her.

Fox, Peppy, Falco, Slippy, Krystal, and Thaddeus and his crew say goodbye to King and Queen EarthWalker and Prince Tricky before powering up the Voyager-27 and launching it toward Corneria. Thaddeus and Krystal comfort each other after learning that their homeworlds were destroyed by a common enemy: the Aparoids. Falco is worried that the Aparoids may invade Lylat, and suggests that they warn Pepper and the Cornerian Army that the Aparoids are on the move. Fox, who is about to contact Pepper, agrees, but he prefers to tell him in person. Then, Fox contacts Pepper and notifies him of the successful mission.

On Corneria, Fox and Peppy warn Pepper about the Aparoids, and Pepper assures them that he'll take the pertinent actions to prepare Corneria for a possible attack. Thaddeus and his crew become official Cornerian citizens and start a new life. On Fox's recommendation, Krystal is accepted into Cornerian Flight Academy. After receiving a check from General Pepper, Fox uses the money to post bail for Chester to release him from prison and Chester reunites with Falco. Another portion of the money is invested in the manufacturing of a new mothership for the Star Fox team. Pepper, Peppy, Falco, Slippy, Bill, Beltino, Chester, Krystal, and Katt celebrate Fox's 24th birthday again to make up for his past birthday which was interrupted by General Pepper's distress call, while they watch the construction of Team Star Fox's new mothership, the Magnificent Fox, at a Space Dynamics Ltd. constructing/manufacturing facility.

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