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.