Twenty-four-year-old Kara Zor-El, who was taken in by the Danvers family when she was 13 after being sent away from Krypton, must learn to embrace her powers after previously hiding them. The Danvers teach her to be careful with her powers, until she has to reveal them during an unexpected disaster, setting her on her journey of heroism.
As Brainiac lays close to death after trying to stop Lex, Supergirl and team soar in to save him, engaging in an epic battle with Gamemnae. After beating Leviathan, Supergirl turns her attention to Lex who has used the Obsidian platform to brainwash half the world to love him and follow him at all costs, no matter what horrible things he does. Knowing how dangerous this makes her brother, Lena enlists the entire team – Alex, J’onn , Dreamer, Kelly and Brainiac – to help, but Supergirl realizes that the only way to truly stop Lex is to sacrifice herself.
As the stakes with Lex are raised higher than ever before, Lena must decide how far she is willing to go to stop her brother. Meanwhile, Supergirl and the team are faced with a challenge unlike anything they've ever dealt with before and it brings Alex to her breaking point.
Supergirl makes a new ally. Lena and Lex battle for control of Luthor Corp.
Supergirl finds an opportunity to escape from the Phantom Zone but it comes with some dangerous strings attached. Meanwhile, Lena joins the Super Friends on a mission but finds she disagrees with their plan of action against the Phantoms and wonders if she is truly ready to be a part of the team.
Nia and Brainy attempt to save Supergirl from the Phantom Zone by time traveling back to Kara's home in 2009. While determined to secure the item needed to help Supergirl, Brainy is worried about keeping a low profile so as not to alter the future timeline. However, when their ship crashes upon arrival, a young Kara Danvers is the first on the scene. Meanwhile, a young reporter named Cat Grant sets her sights on Midvale as she suspects there is a big story in the small town.
Part two of the flashback episodes pick up where things left off - Young Kara experiences kryptonite for the first time, Nia and Brainy are trapped by invading aliens, and a young Cat Grant may be the reason Supergirl never gets out of the Phantom Zone.
As the Super Friends brave the Phantom Zone to bring Supergirl home, each member of the team is confronted by visions of their worst fear.
As Supergirl and Zor-El make their return to National City, they are determined to keep the Phantom Zone behind them and enjoy being superheroes together. Unfortunately, their overzealous efforts backfire, creating a whole new threat to National City.
Kelly meets Joey, a young orphaned alien boy, who is acting out in foster care because he fears there is something wrong with his brother Orlando, who is incarcerated. Kelly asks Kara to help her investigate and they stumble upon abuse at the prison. Meanwhile, Nyxly crashes one of Nia's dreams and asks her for help.
Supergirl intervenes when a building in the Heights that was set aside for low income housing is suddenly at risk to be sold to a major corporation. Supergirl recruits Orlando to help her win over the city, but things go awry when Nyxly shows up. Meanwhile, Nia trains with her mother.
Supergirl and team must stop Nyxly from vanquishing a familiar face from Supergirl's past - Mr. Mxyzptlk. Mxy returns and explains Nyxly's dark history to the super team in the best way he knows how - in song form. Meanwhile, Lena visits her mother's birthplace in Newfoundland, eager to dig into her past but is shocked by the small town's icy reception towards her.
Kelly is horrified when the Ormfell building implodes, injuring many in the community, including Joey. However, her horror quickly turns to frustration when she realizes that the hospital is overwhelmed, people are getting sicker, and no one is coming to help - including Supergirl who is busy fighting Nyxly. Knowing that she can make a difference, Kelly embraces her power and fully steps into her role as Guardian. Joined by Supergirl, Alex, Diggle and team, Guardian leads the way to restoring justice to the fallen community.
Supergirl and team race Nyxly for control of a magical totem that controls courage. Supergirl and Nyxly battle and each get a piece of the totem but learn the first person to pass the test of courage will gain control of the entire thing. Meanwhile, Lena is still struggling to make sense of her newfound gift.
Lena is uncertain about using her magical abilities to help Supergirl retrieve the second totem from Nyxly. William struggles to write a story on the Super Friends that makes both the heroes and Andrea happy. Meanwhile, Kelly is thrilled Esme has found a new home, but things go awry and the little girl's future is put in danger.
Supergirl continues to fight Nyxly for the remaining totems but after Nyxly kidnaps William, Supergirl realizes she needs to take a more proactive stance to keep National City safe. Meanwhile, Alex faces the biggest challenge of her life.
Kara lands her dream story for Catco but when the city is suddenly attacked by a nightmare monster at the same time as her interview, she is forced to take a serious look at her life and decide if she can continue to live as both Kara and Supergirl. As Dreamer takes the lead on the search for the Dream Totem, which can vanquish they nightmare monster in National City, she realizes she needs to ask her sister Maeve for help.
When Lex Luthor appears by Nyxly's side, Supergirl and team must deal with the emotional fallout of facing their two biggest foes at the same time. Alex makes plans for the perfect proposal to Kelly, but work keeps getting in the way.
Supergirl is determined to keep everyone safe from Lex and Nyxly so she doubles down on patrol, especially as Alex and Kelly's bachelorette party is coming up. Alex is torn between duty and finally allowing herself the time to enjoy her new family. Brainy receives heartbreaking news, and William clashes with Andrea over her recent coverage of Lex.
Supergirl and the super friends take drastic action after a loved one is kidnapped by Nyxly and Lex. An unlikely ally steps in to help the team.
Supergirl is joined by familiar faces from the past to help her stop Lex and Nyxly for good. Meanwhile, Alex and Kelly prepare to walk down the aisle.