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Supergirl is mentioned by Hawkgirl in Clubbing, when the latter mentions about a Kryptonian spacecraft that landed near Metropolis with a female inhabitant inside who has yet to be found, serving as an foreshadow for her future appearance.
In New Beginnings, Supergirl contacts Wonder Woman over video call as she battles Giganta and asks her questions about Super Hero High, contemplating whether to go or not. In the special Super Hero High, Supergirl finally arrives at Super Hero High with a crash and has problems controlling her powers. She's helped by both Barbara Gordon and later Wonder Woman who help her adjust. When she accidently hits Bumblebee with her heat vision in a battle against Giganta, she decides to leave Super Hero High to head to Korugar Academy. When the school librarian Granny Goodness tells her to use the off-limits boom tubes, she gets disabled by Kryptonite when Granny Goodness uses the boom tubes to let in the Female Furies to invade Earth. With Barbara's help, who turns into Batgirl, they disable the Furies' mind control, freeing the students and defeating them. Supergirl later recommends Batgirl for enrolment at Super Hero High.
In Hero of the Month: Supergirl, Supergirl is honoured with the Hero of the Month Award by Principal Waller, and gets testimonials from Poison Ivy, Harley Quinn and Batgirl. In Batgirl vs. Supergirl, Supergirl races Batgirl through the school hallways for the last piece of Super Food Cake in the cafeteria. When they decide to share it, Harley eats it. In Hero of the Month: Harley Quinn, she watches Harley's Hero of the Month announcement in the library from a laptop.
In License to Fly, Supergirl admires Batgirl's new Bat-Jet and later helps her to practice by turning her jet at a sharp turn, to help Batgirl learn turning. In Hero of the Month: Batgirl, she cheers for Batgirl, when she is announced as Hero of the Month in Commissioner Gordon's class.
In Doubles Trouble, Supergirl joins Katana as her tennis partner for a tennis competition in the park, against the Flash and Cyborg. When she flies to look for their ball, she encounters the Double Dare Twins robbing a purse and chases after them, eventually capturing them in a hole.
In Hero of the Month: Katana, she makes a background appearance in Weaponomics class as Katana makes a necklace out of chains and metal disks with her sword. In Dude, Where's My Invisible Jet?, Supergirl helps Wonder Woman, Batgirl and the Junior Detectives Society find Wonder Woman's missing Invisible Jet after a visit to the Capes & Cowls Café to attend a feast on Themiscyra. With Harley's help, they find it using invisible ink.
In Hero of the Month: Frost, Supergirl appears in the student lounge, watching as Frost is announced as the recipient of the Hero of the Month award, with other students. In The Blunder Games, she makes a cameo appearance using her heat vision to roast a kebab in the safe zone for the advanced survival skills final.
In Hawkgirl's Day Off, Supergirl, along with Batgirl and Bumblebee treat Hawkgirl to a relaxing day off at the Super Spa. The three remain oblivious when Hawkgirl clashes with Mrs. Clayface and only do so when a spa employee shows them around and tells them that she a regular customer.  In Hero of the Month: Hawkgirl, she makes a cameo appearance attending Bumblebee's surprise birthday party, as shown in a clip within Hawkgirl's Hero of the Month VT.
In The Cheetah Who Cried Wolf, Supergirl appears in the school hallway with Bumblebee as the Save the Day Alarm goes off, before being shoved out of the way by Cheetah. She later appears with Wonder Woman and Batgirl to battle a giant robot, only to discover it was staged by the Cheetah look good as a hero after pondering how Cheetah managed to arrive at the scene first.
In The Ring of Mire, Supergirl makes a cameo appearance clean up the park, along with other Super Hero High students, by using her heat-vision to destroy trash swept up by Bumblebee. In Roomies Return: Frost's Bite, she races other students into the showers, taking all the stalls before an ill Frost. She and other students later accidentally destroy Frost's heater when responding to the Save the Day Alarm. Frost freezes them in retaliation. In Hero of the Month: Beast Boy, she asks Beast Boy how he will celebrate receiving the titular award. He responds by saying, "I'm just gonna chill" and transforms into a sloth.
In Batnapped, Supergirl works on her shop project and shakes hands with Lena Luthor, the new I.T. girl before receiving a distress call from Batgirl. She then uses her jet to fly to an abandoned movie theatre and rescues her from Killer Moth, who was holding her hostage. Batgirl then ties him up with a rope, before they fly home in the jet.
In Tales From the Kryptomites Part 1, she, Batgirl and Wonder Woman work on their vehicle projects and accidentally fires a missile from her jet which destroys Lena's office. The three of them go to the warehouse where Lena lives to tell her in person. While returning to the school, they encounter a Kryptomite which disables Supergirl, and is then shattered by Wonder Woman and Batgirl who then help her return to the school. In Tales From the Kryptomites Part 2, Supergirl responds to a Save the Day Alarm with other students to battle a Kryptomite infestation of Metropolis. Disabled by them, she collapses and is taken away from the battle by Wonder Woman. In Seeing Red, she battles Beast Boy in the Weaponomics room due to the activities of a red Kryptomite roaming the school with anger-inducing powers. Starfire tricks her into using her x-ray vision to tell her where it went. They presumeably stop fighting after Starfire defeats the Kryptomite.
In Around Metropolis in 80 Seconds, she decides to have a street race on motorcycles to settle her speed rivalry with Wonder Woman that Harley also participates in. They get sidetracked when they notice the Double Dare twins robbing a bank and choose to stop them, capturing Margot with her bike's retractable net, while Wonder Woman captures Aliki. This allows Harley to win the race. In For Art's Sake, she helps Principal Waller unveil Silver St. Cloud's painting for the Super Hero High student Art Show fundraiser. When it gets stolen by the Double Dare twins, she flies after them, but is disabled when Aliki throws kryptonite at her. When they try to escape by closing a super-proof emergency wall, she crashes into it while Katana slips through when they both pursue them. Without her help, Katana manages to defeat them.
In The Ares Up There, she attends the Party of Plenty on Themiscyra which gets crashed by Ares and ends up battling him with Wonder Woman, Harley Quinn and Batgirl when he goes on a rampage. When Harley puts the Amulet of Harmonia on him, he calms down and leaves. In Body Electric, she and Wonder Woman fly to arrest Giganta after she goes on a rampage, causing a blackout, and is defeated. They then attend Thunder and Lightning medal ceremony for ending the blackout and hug Batgirl.
In Fresh Ares Part 1, she appears as a patron at Capes & Cowls with Wonder Woman and Batgirl and greets Ares as he arrives to give a peace offering to Wonder Woman. The three later leave for the school when Supergirl hears Harley Quinn cry for help with her enhanced hearing. Upon arriving with Bumblebee, they learn from her that it was a false alarm orchestrated by Catwoman. In Fresh Ares Part 2, Supergirl and her friends return to the city when Ares goes on a rampage after Catwoman steals his Amulet of Harmonia to battle him. Ares knocks her into a building with a radio tower, causing it to tip over. After her classmates manage to subdue him, she appears watching. In Fresh Ares Part 3, Ares breaks free and continues his rampage, and she helps Wonder Woman stop a building from falling over. She taunts Ares by playing keep away with his peace offering over his head with Wonder Woman. After getting blasted by fire from Ares, she and Wonder Woman are left unconscious and vulnerable as Ares tries to finish them, but his rampage abruptly ends when Catwoman returns to him the amulet before he can.
In Fight Flub, she makes a background appearance attending an Advanced Martial Arts class taught by Coach Wildcat, who later directs the class, (excluding Katana and Big Barda) to the sparring mats. In Jetsetters, she makes a cameo appearance using her heat vision to thaw out Wonder Woman's frozen invisible jet with Batgirl.
In Dog Day After School, she detects Kryptonian activity while flying her jet in Metropolis. She later responds to a Save the Day Alarm with Hawkgirl and Beast Boy, noticing a rampaged street. They eventually pursue the cause of the rampage to Capes & Cowls with Catwoman where Steve Trevor directs them to an alley outside the building. There, they learn the cause is Supergirl's Kryptonian dog Krypto, and she reunites with him. In It's a Superful Life, she participates in a holiday toy drive with her classmates before they decide to share themselves for the holidays. She and Bumblebee go to a construction site to give hot cocoa to the workers, warming it with her heat vision. During the school holiday tree ceremony, she decorates the tree with a picture of her Kryptonian parents.
In Ring Me Maybe Part 1, Supergirl attends Hal Jordan's going-away party and defends the super food cake when Solomon Grundy crashes the party and is defeated by her classmates. She later escorts Hal in her jet as he flies to complete his Green Lantern training on Oa. In Ring Me Maybe Part 2, Sinestro arrives on Earth to kidnap Super Hero High students to take to Korugar Academy, and declares his intentions to capture Supergirl. Batgirl tries to warn her to stay away from Earth due to this, but due to poor call reception, she misunderstands her as saying that she needs her on Earth, prompting her to continue the trip back. In Ring Me Maybe Part 3, she arrives on Earth and is captured by Sinestro who intends her to make her his team's captain. In Ring Me Maybe Part 4, she gets imprisoned on his ship, but is rescued along with the other students by Batgirl when she sneaks aboard the ship while Jessica Cruz defeats Sinestro in battle using constructs of Wonder Woman, Batgirl and Supergirl. Later, she gestures to Jessica in encouragement to become a student at Super Hero High with Batgirl and Wonder Woman.
In Gone to the Dogs Part 1, she has a playdate in the park with Krypto and is joined by Batgirl and her new dog Ace. They leave their pets in Batgirl's bat-bunker to investigate a break-in at a jewelry store. While investigating, Supergirl discovers a toy mouse at the crime scene with her x-ray vision and suspect Catwoman as the culprit. In Gone to the Dogs Part 2, Supergirl and Batgirl interrogate Catwoman but leave her after only finding cat toys in her dorm. As they return to the jewelry store to report to Principal Waller that they have not found the culprit, Ace and Krypto arrive with the stolen jewelry. Waller then decides to abolish the school's no pets rule. Later that night, she appears sleeping in her room with Krypto while Roz steals Krypto's collar. In Pets Peeved Part 1, she and other pet owners are threatened with failure by Vice Principal Grodd when their pets fail to work together for a class. Later that night, she contacts Bumblebee and Wonder Woman to investigate Centennial Park Zoo with the other pet owners. There, they battle the Animilitia, where she throws Killer Croc and later battles him again with Bumblebee. She and her classmates are eventually trapped in a kryptonite-laced room in the park by the Animilitia, causing her collapse. In Pets Peeved Part 2, while weakened by the kryptonite, she and her friends are rescued by their pets, who defeat the Animilitia by working together and reunite with their owners.
In Ha-Ha Horticulture, when Ivy's sleeping poppy experiment puts makes the school's students and staff fall asleep, she falls asleep in the garage in front of her jet, with each of her breaths in and out alternately pulling it towards and pushing it away from her respectively. She wakes up with the rest of the school wake up when Ivy and Harley distribute pollen around the school which counteracts the effects of the poppy.
In Truth of the Lasso Part 3, Supergirl attends a school field trip to the Gotham Dentistry museum, but their bus gets caught in a traffic jam due to a rampaging Giganta. As she chases the bus, Supergirl is taken by Harley out of the bus on a detachable buggy to escape her and gets separated from her classmates when Giganta separates them from the bus. In Truth of the Lasso Part 4, after they return to confront her, they learn about Giganta's stolen earrings. Later, they track down their missing classmate Wonder Woman and confront her captor, the Cheetah in the sewer, as she stands down. She later appears walking back from the bus from the dentistry museum with Harley, agreeing that the trip was surprisingly interesting.
In Nevermore Part 1, after racing Batgirl's batcycle hologram to Capes & Cowls, Supergirl leaves the Café with Batgirl and Bumblebee to investigate spontaneous lava eruptions emerging from craters in the Metropolis streets created by Trigon trying to teach Raven magic in the underworld. As the lava erupts, Supergirl and her friends save citizens before she freezes it with her freeze breath. In Nevermore Part 2, she continues to save citizens from the eruptions and successfully solicits Raven for help. Together, they stop a building from falling over before taking more citizens to Super Hero High School before being called to sector seven and introducing Raven to Principal Waller. In Nevermore Part 3, she tries to explain Raven's actions to Trigon when he grounds her by saying "she was only being a hero" only to backfire. As Trigon tries to destroy Super Hero High, she and Batgirl work together to subdue him, tying their super save score. After he breaks free and grabs Batgirl, she tries to free her only to get herself grabbed in his hand and chastised for interfering with his family life. In Nevermore Part 4, Trigon calls Supergirl and Batgirl a bad influence on his daughter Raven, before Supergirl frees them both. She convinces Raven to use her magical powers to stop him, and Raven sends Trigon back to the underworld through a portal. While leaving, Trigon allows Raven to attend Super Hero High. As Supergirl hugs her, she knocks her back, saying she doesn't do hugs.
In Tamaranean Dance Club Part 1, she and her friends stop the Double Dare twins as they rob Lena Luthor's warehouse, with Supergirl destroying a light cable supporting Margot, making her fall to the ground. She and her friends prepare for a surprise dance with Korugar students for Starfire, with Katana making costumes and learning how to dance from Crazy Quilt. Partnered with the Flash for the lesson, she drills him into the ground with her super strength. In Tamaranean Dance Club Part 2, she learns that "dance" is a Tamaranean word for "domination battle" and is later seen defeating Bleez as Wonder Woman calls out dance moves, contributing to Super Hero High victory in the dance. She later has a meal at Capes & Cowls with Katana, Wonder Woman and Starfire.
In By the Yearbook, she makes a cameo appearance making a face with Batgirl as Harley takes a picture for the Super Hero High yearbook.
In Spell-shocked Part 1, Supergirl has lunch with Wonder Woman, Bumblebee and Raven and asks Raven how far she can take a portal. After returning from the portal, she tells Bumblebee and Supergirl of a terrible vision of the future she saw. She then accompanies Batgirl and Raven as they try to ask Darkseid for help understanding the vision, but to no avail. In Spell-shocked Part 2, she stops a large globe sent rolling by the Book of Legends as it rampages across the school. She then helps Batgirl, Wonder Woman and Raven stop the Book of Legends, eventually finding it the cafeteria, where she helps blast through an assault of pots and pans sent by the book with her heat vision. After the book is defeated, she asks Raven about the vision again, but again without success.
In Bottle Episode, after attending Poison Ivy's Earth Day recycling presentation, finds the Bottle city of Kandor left in her locker by Superman. After stopping Harley from shaking it, she jumps through the trash disposal chute after Parasite throws the bottle down it. She uses her powers to save it from being destroyed by the trash incineration system, but eventually loses it when it falls through a hole. After returning to the halls, she finds that it was saved by a bottle procurement mechanism installed by Poison Ivy in the trash processor. She later has Grodd store the city in a secure location. In Career Day, she flies through the school halls with Wonder Woman in excitement for Career Day at the school and watches as Wonder Woman gets assigned to janitorial work.
In Mood Ring, she attends a Phys Ed class and blows Star Sapphire with her freeze breath, damaging her power ring and getting hit by its red anger element. After the class ends, she chases Beast Boy with her heat vision in the school hallway and later picks up the Flash, ready to throw him on the ground. When Star Sapphire pairs her with Principal Waller and Grodd, both affected by the violet love element, they return to normal. In My New Best Friend, she confronts Catwoman and an amnesic Batgirl with Poison Ivy and Hawkgirl after they steal Principal Waller's laptop near the Lady Justice statue. Supergirl swats a batarang away when Catwoman throws it at her, hitting Batgirl in the head and restoring her memories, allowing her to put Catwoman under school citizen's arrest. She and her friends later have lunch at Capes & Cowls.
In Anti Hall Monitor Part 1, she uses Batgirl's anti-hall monitor app to avoid Hawkgirl's hall monitoring with Wonder Woman after Harley spills its secret. In Anti Hall Monitor Part 2, she is seen among the many students trapped in a superpower-proof room by the monster created by the anti-hall monitor app's artificial intelligence. After Hawkgirl defeats the monster, she and her classmates are zapped back into the school foyer.
In Haunted Harley, she attends an algebra quiz in Dr. Seid's class before it is interrupted by a false Save the Day alarm orchestrated by Harley. She later hears Bumblebee's cries for help with her super hearing in a school hallway with Batgirl, and they save her from nearly being sucked into a fan with her suit stuck on shrank. She uses her x-ray vision to identify the damaged part of her suit which Batgirl repairs, restoring her size.
In the first part of All Pets Are Off, Beast Boy enters the Super Hero High pet show as Supergirl's pet as an undercover green poodle after Krypto goes missing, and is the only pet to fail to win a medal. Artemiz suddenly appears and engages the pet owners, and manages to steal the remaining pets in the Battywagon. She notices Artemiz also stole Krypto with her x-ray vision. In the second part, after Beast Boy escapes the Battywagon, Supergirl rescues him from being run over by a truck, and uses her freeze breath to freeze the road, destabilizing the Battywagon and allowing the pets to break free and defeat Artemiz. She and the other pet owners then reunite with their pets.
In The Wobble, she performs a gymnastics routine in the SHH gym and receives a perfect score and comforts Wonder Woman when she fails to do the same, advising her that a mistake is a chance to learn something new. When attempting another routine, she is attacked by Bleez, who is angry at the judges for how she was judged in a previous meet with Korugar Academy. After she exchanges blows with Bleez, Wonder Woman defeats her by using Supergirl's advice. Supergirl then tries to give similar cheery advice to Bleez, much to her irritation. In Target Practice, Supergirl plays frisbee with Wonder Woman in the skies before introducing the game to Starfire. After relocating to the park, she helps Starfire learn to throw it. When she tries to find the disks thrown into the bushes, she faints due to the presence of Kryptomites, who carry her away. After Starfire and Wonder Woman defeat the Kryptomites, she gets rescued and continues to play frisbee with them. She then asks is Starfire has ever tried yo-yo before, when they see Beast Boy playing with one.
In the first part of For the Girl Who Has Everything, Supergirl gets a "C" on her perfect world model assignment after refusing to let her partner Harley participate on it, ostensibly so she would not add chattering teeth to it. After Batgirl tells her that only in a perfect world, they can do everything themselves, she and her friends later answer a Save the Day Alarm in the school garage, and Supergirl faints as Kryptomites tripped the alarm looting the garage. She is then brought to her room to sleep by Wonder Woman and Poison Ivy puts in a Kryptonian plant they found with the kryptomites to cheer her up. In the second part, she gets attacked by the plant, and dreams of Vice Principal Grodd giving her an "A" on the aforementioned project, and telling her that she is not only immune to kryptonite, but also the school has been named after her. When she notices that there is none of her friends are there, Grodd tells her that as the world has become perfect and she does not need any one other than herself, similar to what Batgirl told her. She battles Grodd, and is trapped inside a plant that emerges from the ground. After her friends defeat the plant monster and apologizing for worsening her day, she wakes up and tells then they are "the only reason why her days are any good".
In Missing Martian, Miss Martian overhears her planning a plot involving poisonous gas with Katana and Wonder Woman in the cafeteria. Later that night, she follows them to the park and confronts them, only to realize they were luring her into a surprise birthday party, as they knew she would never agree to one. Supergirl also explains to her that she knew she was eavesdropping while invisible as she heard her heartbeat with her enhanced hearing and they saw her floating sandwich.
In the first part of Fortress of Solidarity, she attends a winter holiday celebration at the school and compares it to winter feast, a Kryptonian celebration. When she mentions it includes watching the "night rainbow sky", Batgirl tells her about the aurora borealis, a similar earth phenomenon. Seeing the other students enjoying the ceremony with their families, Supergirl feels lonely as the Kents are at an agriculture convention. She decides to leave for the arctic to see the aurora borealis to simulate winter feast and is spotted flying away from the school by Batgirl. Upon arriving and appreciating the aurora borealis, she gets attacked by Captain Cold who plans to use her kryptonian crystal to start a new ice age. He weakens her by shooting her with kryptonite. In the second part, Batgirl, Wonder Woman, Frost and Mera arrive to rescue her and battle him, and Batgirl tells that the Kents left the convention early to be with her. After Frost and Mera freeze and defeat him, they enjoy the aurora. When she plants her crystal in the snow, it creates a Fortress of Solidarity. She and her friends enter and engage in a group hug.
In the first part of My So-Called Anti-Life, she attends Dr. Seid's math club and does a multiple choice test, after which Dr. Seid uses Harley's answers to solve the anti-life equation and transform into Darkseid to conquer the world. In the second part, he attacks the math club before leaving to corrupt the school amethyst to use the equation to remake the world in his own image. Supergirl and Starfire are transformed into clone of Darkseid when they fly up to stop him. In the third part, after most of the school has also been transformed, the remaining students apply Batgirl's idea to undo the equation by adding more variables by restoring the individuality of the clones, with Harley turning Supergirl back by putting on her cape. As the effects of the equation are undone, Supergirl helps defeat Darkseid before he retreats. She then stands by Batgirl as she says that they will be ready and waiting if he returns.
- "New Beginnings"
- "Super Hero High"
- "Hero of the Month: Supergirl"
- "Batgirl vs. Supergirl"
- "Hero of the Month: Harley Quinn"
- "License to Fly"
- "Hero of the Month: Batgirl"
- "Doubles Trouble"
- "Dude Where's My Invisible Jet"
- "Hero of the Month: Frost"
- "The Blunder Games"
- "Hawkgirl's Day Off"
- "Hero of the Month: Hawkgirl"
- "The Cheetah Who Cried Wolf"
- "The Ring of Mire"