Princess Celestia and Princess Luna decide to retire and hand off the ruling of Equestria to Twilight Sparkle and her friends, which sends Twilight into a tailspin of self-doubt. Meanwhile, an ancient villain bands together a legion of nefarious characters to conquer all of Equestria, challenging Twilight Sparkle and the rest of the Mane 6 to step in and save the day.
As Twilight and the rest of the Mane six struggle to come to terms with the destruction of the Tree and Elements of Harmony, King Sombra sets his sights on conquering all of Equestria.
Twilight and Shining Armor pit their wits against each other to settle a long-standing sibling rivalry, but they soon discover they are not the only competitors.
Smolder returns to the Dragonlands with Spike and Fluttershy to help cheer up her sensitive brother, but when they arrive they discover the dragon eggs aren't hatching.
Starlight Glimmer relishes her role as school counselor and encourages the students to come to her anytime about anything, but she becomes overwhelmed and learns a lesson.
When Pinkie Pie needs to find her life's purpose, she seeks out her old friend Cheese Sandwich, however she soon discovers that the unimaginable has happened.
Twilight's hopes of keeping her Trivia Trot winning streak alive are waylaid when she's unexpectedly paired up with Pinkie Pie, who has never been to a trivia night before.
When Starlight is told that she will run the School of Friendship after Twilight becomes the ruler of Equestria, she must choose a Vice Mare, putting her friendship with Trixie to the test.
When a previously unheard-of author writes a novel trashing Daring Do, exposing her as a real pony, and praising Dr. Caballeron, Rainbow Dash rushes to defend her friend, while Fluttershy is more sympathetic to the "misunderstood" Caballeron.
When the Cutie Mark Crusaders are magically transformed into grown ups, they discover that growing up the right way means gaining experience and wisdom that simply can't be rushed.
Twilight Sparkle and friends tell a story about how Twilight had to make a difficult decision when Celestia and Luna retire and hand the throne to Twilight who must choose to either be the rightful ruler of Equestria or stay in Ponyville with her friends.