Eight years after Princess Celestia death, the Celestia Act grants the Ponyville Police Department powers which nearly eradicate organized crime. Feeling guilty for covering up Celestia’s crimes, Princess Twilight Sparkle writes a resignation speech confessing the truth but decides not to use it. Mare do Well has disappeared, and Applejack has become a recluse. Cat burglar Rarity obtains Applejack’s hoofprints from her home, kidnaps a congressman, then disappears. Rarity hands Applejack’s hoofprints to Silver Shill, an assistant to Applejack’s business rival Flam, in hope of having her criminal record erased. He double-crosses Rarity, but she uses Silver’s stolen phone to alert the police to their location. Twilight and the police arrive to find Silver, and then pursue his mens into the sewers while Rarity flees. A masked militant named Featherweight captures Twilight. Twilight escapes and is found by Spike, a once-orphaned patrol officer who has deduced Mare do Well’s true identity from their similar backgrounds. Twilight promotes Spike to her assistent, with Spike reporting directly to her.
 
Apple Family is unprofitable after Applejack discontinued her fusion reactor project when she learned that the core could be weaponized. Later, Featherweight attacks the Ponyville Stock Exchange, using Applejack’s hoofprints in a transaction that bankrupts Applejack. Granny Smith, concerned that Applejack has not moved on from being Mare do Well, reveals to him that Caramel had intended to marry Celestia before he died. Granny Smith then resigns in an attempt to dissuade Applejack. Fearing that Flam, Feartherweight’s employer, would gain access to the reactor, Applejack asks Apple Family board member Aunt Orange to take over her company. After being promised the software to erase her criminal record, Rarity agrees to take Mare do Well to Featherweight but instead leads him into Featherweight’s trap. Featherweight uses the venom, a highly addictive super-steroid, to turn into Bulk Biceps reveals that he intends to fulfill Starlight Glimmer mission to destroy Ponyville with the League of Shadows remnant. He engages Mare do Well and delivers a crippling blow to her back, before taking him to a foreign, well-like prison where escape is virtually impossible. The inmates tell Applejack the story of Starligh’s child, born in the prison and cared for by a fellow prisoner before escaping—the only prisoner to have ever done so. Applejack assumes the child to be Featherweight.
 
Meanwhile, Featherweight lures Ponyville police underground and collapses the exits with them in it. He kills Mayor Mare and forces an abducted physicist, Flash Sentry, to convert the reactor core into a nuclear bomb. Featherweight uses the bomb to hold the city hostage and isolate Ponyville from the world. Using Twilight’s stolen speech, Featherweight reveals the cover-up of Celestia’s crimes and releases the prisoners of Blackgate Penitentiary, initiating a revolution. The wealthy and powerful have their property expropriated, are dragged from their homes, and are given show trials presided over by Princess Luna, where any sentence means likely death.
 
After months of recovery from his injury and re-training, Applejack escapes from the prison and enlists Rarity, Spike, Orange, Twilight, and Apple Bloom to help stop the bomb’s detonation. While the police and Featherweight’s forces clash, Mare do Well defeats Bulk Biceps, but Orange intervenes and stabs Batman, revealing herself to be Night Glider, Starlight’s daughter. Night Glider escaped the prison aided by her fellow prisoner and protector, Bulk Biceps. She plans to complete her mother’s work by detonating the bomb and destroying Ponyville, but Twilight blocks her signal, preventing remote detonation. Night Glider leaves to find the bomb while Bulk Biceps prepares to kill Mare do Well, but Rarity kills Bulk Biceps with the cannons on the Batpod. Mare do Well pursues Night Glider with the Bat, an aircraft developed by Apple Bloom, hoping to bring the bomb back to the reactor where it can be stabilized. Night Glider’s truck crashes, but she remotely destroys the reactor before dying. With no way to stop the detonation, Mare do Well uses the Bat to haul the bomb over the bay, where it detonates.
 
In the aftermath, Mare do Well is presumed dead and is honored as a hero. With Applejack also presumed dead, Sweetie Apple Acres is left to the city to become an orphanage, and Aple’s remaining estate is left to Granny Smith. Twilight finds the Bat-Signal refurbished. While visiting Canterlot, Granny Smith imagine Applejack whit a family. Spike (AKA Humdrum) resigns from the police force and inherits the Batcave.