After the changelings were driven from Canterlot, they returned to the Hive. Celestia and her mages weren’t done with the changelings. They found a way to make artifacts that could see through a changeling’s disguise and reveal the creature underneath. She also sent the artifacts to the Diamond Dog, Griffin and other nations. That meant that the Hive couldn’t get emotions from other nations too. The Hive began to implode. All sorts of changelings were drained to feel the growing hunger for emotions. A changeling princess came up with a device that could see into another world. This world had strange creatures that seemed to have similar expressions to ponies. After a meeting with the Queen, she was given what she needed to expand her research.
Margot Sommerholt, a wizard working for an alien organization is sent to work with the FBI to stop a terrorist attack. Eventually she senses some alien magic and shoots a changeling disguised as a teenager. This doesn’t stop the attack and she is forced to leave the building with the other people. While on the way out, she helps a fallen child. That delays her enough so she gets caught within the device’s explosion. Before she passes out from the pain, she sees two blue hooves wrap around her.
Margot wakes up in Equestria as a pink coated and blonde haired unicorn. Margot finds out that her powers are gone. She adapts to being a four legged creature and meets Cheerilee who briefs Margot on the current situation. Cheerilee also tells Margot to go see the Prophetess in Lower Canterlot if she wishes to go home. Later on Margot is introduced to some ponies that will accompany her on her journey. Far Traveler, a caravan leader. Skybreeze Cloud, a disgraced mage from Hoofvard and three fillies that call themselves the Sky Hoof Crusaders. After the SHC do a miracle and provide food, the group sets out for Lower Canterlot.
On the way they have some adventures and save a changeling named Nga'Devro from some zombie pony enemies called Remnants. At the outskirts of Lower Canterlot, Margot meets Empress Razorhoof, the leader of the gleaners.
Empress Razorhoof tries to mess with Margot’s mind. She wants Margot to feel isolated and powerless. That attempt almost works except for an unknown being that talks to Margot. Margot rejects the Empress’s mind magic. Empress Razorhoof leaves while a group of creatures from Lower Canterlot gallops up to them.
Margot meets with the Princesses, Applejack and Rainbow Dash. She finds out that the Prophetess has been kidnapped by gleaner creatures called shriekers. Skybreeze and Margot go to a magical archive to get some books for research. There Margot falls asleep and gets a vision of Pinkie Pie in a deep pool of water. After talking with the archivist. Margot and Skybreeze go to a research tent where Margot gets her powers back. Later on, Margot meets Skybreeze’s sister, Scry. She works with Scry and helps them find out what happened to the Prophetess. After some planning and spell casting, Margot, Skybreeze, Rainbow Dash and a group of changelings go to Skyshriek Tumult, the home of the shriekers. It used to be called Cloudsdale and the region was the home of many pegasi.
The Prophetess is saved but Rainbow Dash is severely injured. After another meeting with the Princesses and some spell casting, they find out where Fluttershy is. Margot finally gets a chance to talk to the Prophetess. The Platinum Squad, an elite group of ponies taught by Luna lead this rescue. They defeat the gleaner corrupted timberwolves and free Fluttershy though a large part of the Everfree is in flames. The group returns back to Lower Canterlot to plan and cast spells.
Pinkie Pie is in an area called Melancholy Marsh and the group has to gallop there. This time Princess Chr’Aya joins the group. Part of the way to the marsh, the group is almost overcome by the sadness but a new unicorn named Jerome Siklis saves them. He is a human wizard who specialized in mind magic. The alien organization brought him in when Margot disappeared. Jerome was investigating the mall with another FBI agent when gleaners came and attacked them. Before the Gleaners could kill Jerome, he was transported to Equestria to help Margot.
Jerome works with Margot to find where Pinkie Pie is and also casts a spell to keep the ponies safe from the crushing sadness. When they reach Pinkie’s pool, Far dives in and gets Pinkie. Also the group has been hearing the hoofbeats of a giant pony. Pinkie is hugged and returns to her old self just as GrinGrinder appears. GrinGrinder tries to crush the group with sadness but they resist. Pinkie uses her laughter and converts GrinGrinder. Foulshaper moves up on them and GrinGrinder stays behind. The group gallops away and hears GrinGrinder’s last cry of defiance.
The group gallops out of the marsh and finally meets the Train, a biomechanical horror made by Foulshaper. The Train sends a bunch of remnants and gleaners to attack them before heading south. Far flies south to warn Ponyville while Nga'Devro heads north to get help from Lower Canterlot. The rest of the group fight and retreat north until Luna comes with an army to help them. After losing some ponies to remnants, Luna’s army defeats them and the group is sent in a flying carriage back to Lower Canterlot.