Following Earth's destruction, the Fugitoid takes April, Casey, and the Turtles, back in time six months to before the Triceraton invasion, with the objective being to stop the Triceratons before they acquire all three pieces of the Black Hole Generator and use it on Earth. When shown the Fugitoid's armory, April suits up in a yellow jumpsuit with a handheld blaster to use alongside her Tessen fan from Master Splinter. When she first steps outside of the Ulixes, amazed by space, she just wants to float away and never go back to the ship, but when the ship is besieged by asteroids, she is forced to return to it before the ship has to land on the planet Varanon for repairs and refueling. While exploring the spaceport, April comes across a valuable mood crystal, but when it is knocked out of her hands and shatters on the ground, she tries to apologize to the alien merchant, who assures her that it is no problem as it was on sale, but for a very high price of alien currency, which April has none of. As a result of April being unable to pay, the merchant becomes hostile, and chases after her with a laser blaster, demanding she pay for the damaged goods, until April runs into Lord Dregg, forcing the merchant to forget about April owing her for the mood crystal and run for her life to avoid Dregg's wrath. When Dregg takes on the Turtles, Casey, and April himself after his Vreen bodyguards are slain, he captures April and wonders if she is of the Terran race, AKA humanity. April replies that she is, and on Earth, her kind squash bugs, which only enrages Dregg to where he tries to eat her, before she blasts him in the mouth with her blaster, forcing him to release her, and allow her, Casey, and the Turtles to flee back to the Ulixes and escape Varanon, before Dregg gives pursuit in the Hornitron and sends more of his Vreen drones to attack the Ulixes. They are all eliminated, and the Fugitoid is able to warp the ship to safety, but it is out of the frying pan and into the fire as April and the others find themselves surrounded by Triceraton Raptor Fighters, having emerged from warp right on top of the Triceraton Armada.
When April and the rest of the gang are shot down by Triceraton Raptor Fighters, they crash on the ice-cold moon nearby, along with the Salamandrians that Raph and Mikey later name Mona Lisa and Sal Commander. With the Ulixes in need of major repairs, and the life-support on their suits only having a few hours on them before it shuts down and leaves them to perish in the subzero weather, they attempt to find a source of irrilium metal to repair the Ulixes and save their lives. They soon run into the Salamandrians, and a battle ensues when the Salamandrians take Leo's offer of cooperation as one of their signs of combat by mistake. After the Salamandrians leave them after they are buried under snow, Raph breaks off to still try and broker an alliance with the Salamandrians, helping to save them from several Ice Dragons, allowing the Salamandrians to help save April and the others from more Ice Dragons. They soon find the irrilium and take it back to the Ulixes, while losing the pursuit of the Ice Dragons thanks to Casey's photon pucks. However, once back at the Ulixes, April and the others' life-support in their suits finally run out of power, and they begin to pass out and succumb to the freezing temperatures, but the Fugitoid is able to repair the Ulixes in time and get everyone safely back aboard, saving their lives, including April's. With new allies in the Salamandrians, April and the others take off to resume their search for the Black Hole Generator.
As the gang continue their search for the Heart of Darkness, they come across an abandoned space ship and decide to investigate. As they do, April has a bad feeling about it, and Casey wishes to see some action, like some zombies. Unknown to the gang, a hyper cube carrying a genie-like space alien called Wyrm, overhears Casey and grants his wish, reanimating the crew as zombies for Casey to fight before the gang is able to retrieve the hyper cube and return to the Ulixes. Back on board, despite April's objections, and mostly due to curiosity, Casey releases Wyrm, who soon manages to get the gang to make two more wishes, releasing him from his hyper cube imprisonment and allow him to run rampant and make April and the Turtles' lives a nightmare, until Casey offers to join him and requests one more wish before finishing April and the Turtles off. Unfortunately for Wyrm, Casey's extra wish is to undo recent events, putting everyone right back to before Casey made his first wish, where right as he starts to make it, April intervenes, having a gut feeling that something is not right and Casey should not say another word. With that, the gang return to the Ulixes, leaving Wyrm trapped in his hyper cube prison, pleading for them to make a wish and let him out, to no avail.
Continuing their search for the Black Hole Generator pieces, April is being trained to hone her psychic powers with the Fugitoid. Soon, the gang are attacked by a bounty hunter hired by Lord Dregg to attain his revenge on them by the name of Armaggon. An attempt to escape him leads them to an old space station that, unknown to them, had been shut down by the crew as the station's A.I., Overmind, had deemed all organic life to be a threat and wanted to eliminate it. As April and the others investigate, Overmind manages to possess the robotic body of the Fugitoid, while Armaggon activates the station's robot assembly line to create an army of VX3 Warbots to eliminate April and the others. Soon, April, Casey, and the Turtles are captured by Overmind to be made into loyal robot drones to serve him, but are saved by Armaggon after Dregg wanted them brought back alive. Realizing the only way to stop Overmind is to get the Fugitoid back in possession of his body, April uses her psychic powers to reach Prof. Honeycutt's human mind within the Fugitoid's body, allowing him to retake control, before using his Fusion Generator to overload the station's power systems and cause it to self-destruct. April and the rest of the team, sans Leo, are able to make it back the the Ulixes and escape, and Raph is able to rescue Leo after Armaggon is presumed dead after crashing into, and destroying, Overmind's hard drive. The Fugitoid soon locates the Triceraton Armada, and as April and the others resume their pursuit, none of them realize that Armaggon is still alive, and still after them to collect his bounty.
Arriving at the planet of the Aeons where the first piece of the Black Hole Generator is located, April soon finds herself struggling to maintain order among the Turtles and Casey when they start lashing out at each other due to the planet's dark atmosphere affecting their anger and tempers, until they soon locate an Aeon artifact that directs them to the temple where the piece is located. Unfortunately, Captain Mozar and his Triceratons arrive, and despite their best efforts, April and the Turtles lose the first piece to the Triceratons, who then trap them in the temple to perish while Mozar escapes with the first piece. However, using her psychic powers, April is able to locate the Aeons' Sol Star, and return it to the top of the temple, where its power restores the planet to its pristine state and turns the Aeons back from their corrupted forms. As a token of their gratitude, the Aeons bestow a piece of their Sol Star to April, promising that it will bring her and the Turtles luck and great power in their quest, before taking their leave. Back aboard the Ulixes, April listens to the Turtles talk about how the first piece of the Black Hole Generator was able to corrupt the Aeons, and then looks back at her gift from them with a smile.
Following a lead on a criminal contact the Fugitoid knows, Vrax Belebome, who has knowledge of the schematics of the Triceraton Armada's flagship, April and Casey have to stay behind on the Ulixes while the Fugitoid and the Turtles travel into the cantina where Vrax is waiting for them due to how the cantina does not take kindly to Terrans. After the Turtles and the Fugitoid return empty-handed due to Vrax having been angered by Mikey before they made the deal and increasing the cost to twice as originally agreed upon, April soon finds herself being asked to help save Mikey as his brain has been invaded by microscopic aliens know as the Neutrinos, sent by Vrax to extract what knowledge Mikey has on the Black Hole Generator for him to sell to the highest bidder, such as Lord Dregg. While Mikey's brothers are sent into his mind to help save it, April uses her psychic powers with the aid of the Fugitoid and Casey to help direct the Turtles to where Mikey's true self resides in his brain: In his imagination. In the end, the Neutrinos are defeated, and April watches as Mikey crushes their ship underfoot, before the Turtles return to the cantina and get the schematics for the Triceraton flagship from Vrax, with Mikey getting some retribution of his own for what Vrax put him through.
With the schematics of the Triceraton flagship in their possession, the team prepare to take back the first piece of the Black Hole Generator. April is asked to stay on the Ulixes with Casey and the Fugitoid to oversee the Turtles' infiltration of the flagship. However, things fall apart when the Turtles are caught by newly-promoted Admiral Mozar and then sentenced by Emperor Zanmaron to be pitted in the Tri-Arena. April is forced to infiltrate the flagship with the Fugitoid and Casey, but upon being caught by Mozar after getting past the security, April and Casey head for the main armory while the Fugitoid is captured and brought before the Emperor. Avoiding the guards as they head up to watch their champion, Zeno, take down the Turtles, April and Casey reach the armory, where April uses the gift from the Aeons to focus her psychic powers to open the doors. Once inside, April finds several of the Triceraton devices that were used to capture Casey and some of their allies during the invasion of Earth, and uses one to carry the first piece of the Black Hole Generator out of the armory, only to soon run into two of the guards, who force April and Casey to run for it with the piece as they shoot after them. April and Casey then run into the Turtles and the Fugitoid, who had managed to escape thanks to Zeno, and had taken Emperor Zanmaron hostage to ensure their escape. In the collision, the Emperor's crown is knocked off, and though April and Casey's pursuers hold their fire under the threat of hitting the Emperor in the crossfire, Zanmaron and Mozar order them to forget about the Emperor and stop the Turtles. April leads everyone to the nearest airlock, telling them to hold their breath as she hits the button to open it and suck them out into space. As everyone does as she told them, April uses her powers and the Aeons' gift to summon the Ulixes' stealth ship, allowing them to escape back to the Ulixes, and then make good their getaway with the first piece of the Black Hole Generator before they could be stopped by Triceraton Raptor Fighters. With the first piece secured, April asks the Fugitoid where the other two pieces might be, and as the Fugitoid has a good idea where they are, the team set off to find the rest of the Heart of Darkness and destroy it before the Triceratons can use it on Earth.
While the Turtles and the Fugitoid head to Dimension X to meet up with the Utroms, April and Casey have to stay behind in the Ulixes, much to their anger. April tries to read a magazine to distract herself from being unable to go see the Utroms with the Turtles and Fugitoid.
Now with the knowledge of the location of the other two pieces of the Heart of Darkness from the Utroms, April and the others set course for the Cosmic Ocean of Varuna. As they arrive, they encounter the guardians of the second piece, the Daagons, who are at first hostile until the Fugitoid presents the symbol of the Utroms, at which point, the Daagons stand down and escort April and the others to their leader, Hiidrala, who explains that if they want the second piece, they must prove themselves worthy to its guardian, Cthugga, first. After they set off, they are attacked by Armaggon, who manages to get aboard and take Leo hostage, forcing April to drop her blaster and surrender. As they approach where Cthugga resides, April uses her psychic powers to detect it, and soon has to hang on for her life as they try to escape the behemoth, screaming when it looks like it will eat them before it crashes into an asteroid and allows them to hide from it until she is able to sense it leave with her psychic powers again. The Daagons soon arrive to apprehend Armagggon, and upon returning to Hiidrala, April and the others plead for another chance to prove themselves, but Lord Dregg and his Vreen arrive to claim the second piece themselves. April joins in the battle, fighting off Vreen drones, until Hiidrala summons Cthugga to devour Dregg and Armaggon. Without Dregg's hive mind, the Vreen are forced to retreat without further conflict, and Hiidrala awards the second piece to the gang for their heroism and assistance in protecting her kingdom. With two pieces in their possession, the gang set off to find the third piece, though April is saddened to be leaving the Cosmic Ocean because of how beautiful it is in her eyes.
April was fast asleep with Casey on the Ulixes during when the Turtles are summoned by their 1987 counterparts to stop Krang and Kraang Subprime with Krang's plan to destroy the 1987, 2012, and Mirage universes with Krang's weapon, the Dimensionalizer.
When the Triceratons are able to track down the Ulixes and attack it in an attempt to take back the first to pieces of the Heart of Darkness from the gang. April is horrified when debris from the Rock Rocket hitting the Ulixes decapitates the Fugitoid. When the Skeevix Virus is unleashed on the Ulixes, April goes with Casey and one of the Turtles to track it down, only to find them attacking the Ulixes' power core after evolving, having to kill all of them after they manage to disable the power core. Soon after, when the pilots of the pursuing Raptors attack the ship directly, April is able to fight off the lead pilot before the Fugitoid finishes him off, but the other two pilots manage to escape with the pieces of the Heart of Darkness. Despite the loss, April remains hopeful with finding and destroying the final piece before the Triceratons get it first.
As the gang continue their search for the final piece of the Black Hole Generator, they receive a call for help from Mona Lisa as Sal Commander has been captured by Armaggon and taken to Lord Dregg's home planet of Sectoid 1. Once they land, it is not long before April has to take Donnie back to the Ulixes with the Fugitoid after Donnie is stung several times by a Xaxx Bee and infected with its venom. Worried for his well-being, once Donnie is given the anti-venom and cured, April gives him a kiss to show how relieved she is that he's alright. Together, they travel to Dregg's castle, where April creates a distraction with her psychic powers to cause Dregg to attack Armaggon under the pretense Armaggon threw something at Dregg intentionally. Once they are busy, April rescues the others from the Scorpinoid, and once the Fugitoid blasts a way out, they return to the Ulixes, only to have to do battle with Dregg until he is defeated by Raph and they are able to get an severely injured Mona aboard the Ulixes and treat her injuries. April is witness as Sal Commander offers his and Mona's deepest apologies for betraying them and ask for their forgiveness.
As the team make their way to Magdomar, home of the guardian of the final piece of the Black Hole Generator, Tokka, they find that Mozar and the Triceratons are already there and beginning their search of the planet for the piece. Thankfully, the team find it first, but are attacked by Lord Dregg. He manages to damage the Ulixes, causing it to crash-land, and leaving April, Casey, and the Turtles to go after the piece on foot, where they are attacked by Dregg again. During that fight, April uses her psychic powers to turn several of Dregg's chest missiles back on him. They later get into a quick scuffle with Mozar and his men, but escape to go after the final piece again, only for Tokka to awaken at that point to defend the piece. While the Turtles go for the piece, Raph leaves an baby alien turtle he befriended named Chompy Picasso with April and Casey, who soon find that Chompy is Tokka's baby, and April returns Chompy to Tokka without trouble. Unfortunately, though the Turtles free the stuck piece, Dregg steals it and delivers it to the Triceratons. As the gang set course back home to Earth, April discovers Mozar hacking into their communications to gloat at how he plans on using the Heart of Darkness on the Earth, much to her and the others' horror.
With the Ulixes returning to the Milky Way and Earth, April is happy that she'll be able to see her father again after so long, before being reminded that if they fail to stop the Triceratons now, Earth is lost forever. Sensing something else on Prof. Honeycutt's mind, April asks him what's wrong, and the Fugitoid confesses to the Heart of Darkness being his creation, not the Kraang's, having been paid off by Kraang Subprime to convert it from an energy generator to the doomsday weapon it now was to further fund his research. April is shocked by this, and can't believe it. She's even more worried when Leo, in a desperate and furious mood after learning that revelation, goes after the Triceraton flagship alone, and is nearly killed as a result while the Ulixes nearly crashes on Mars. Once Leo is retrieved and resuscitated, they continue to Earth, just in time to watch their past selves already engaging the Triceratons in combat to stop the Heart of Darkness like last time with the Mutanimals, Muckman, Mondo Gecko, and Master Splinter. When the Fugitoid explains his plan on having April, Casey, and the Turtles aid their past selves while he retrieves his doomsday device, April senses that the Fugitoid is lying about his real intentions. Instead of telling them the truth, he ejects them from his ship when they refuse to cooperate, leaving them to carry out his original orders. Meeting up with her past self, April is able to help overpower Captain Mozar when he beams down to confront everyone after Leo destroys the detonator, disarming the Heart of Darkness, then bear witness to the Fugitoid's true intentions as he sacrifices the Ulixes, and himself, to destroy the Heart of Darkness and the Triceraton flagship once and for all. Saddened by his sacrifice, April then focuses on how there are now two of her on Earth, interested in the prospect of having a twin sister, before the past Ulixes and Fugitoid arrives to pick up the past Turtles, April, and Casey, to take on a journey through space, thereby cleaning up any loose ends in regards to two of the Turtles, April, and Casey being on Earth, and allowing the future April, Casey, and the Turtles, to return home with Master Splinter and all their allies, glad to know the Earth is safe from annihilation for good, and they've got a lot to tell their friends and family in the days to come.