- Thorax - Appearing in A Canterlot Wedding, he runs into the Mane Six and the Dragon-Worlders while they're fighting to save Canterlot. Due to being more reluctant to fight than his brothers and sisters, he quickly joins them and helps to bring Chrysalis down by stealing the love energy she took from Shining Armor, which then leads to him dethroning Chrysalis here and being honored for helping save Equestria.
- Pharynx - Also appearing in A Canterlot Wedding, he'll be Chrysalis' second-in-command, facing down his brother during the invasion, and going unchanged for a long while after he is caught and later recruited into Spyro's group. (See below WMG for more information on his recruitment.)
- Smolder - Appearing alongside her brother in Dragon Quest, she forms a bond with Spike that leads to her moving to Ponyville much earlier on.
- Ember - Also appearing in Dragon Quest with her father, Lord Torch, both of whom would encounter Spyro and recognize him due to his name becoming feared among all the dragons following the events of Dragon War.
- Fancy Pants - Appearing in The Best Night Ever with his wife, Fleur de Lis, as one of the nobles attending the Gala.
- Spoiled Rich - Appearing in Call of the Cutie. See below WMG for further information.
- Moondancer - Appearing during A Canterlot Wedding as one of the ponies invited to Cadence's wedding, either as a guest, or as one of the bridesmaids, and will Twilight will not remember her until she's reminded by Minuette.
- Discord - When he steals the Elements of Harmony and leaves his riddle behind, the Dragon Worlders quickly act to solve it. With the riddle being solved by the Dragon Worlders before the ponies go into the labyrinth, Spyro and company then return to Ponyville. There, Discord tries to corrupt the Mane Six so they can't use the Elements on him, but it doesn't last long because Spyro is there to dish out some more Dope Slaps. Afterwards, Discord tries to pull the same mind games on Spyro himself, only for the dragon break through all of his tricks due to his one-track mind before giving the God of Chaos a comical No-Holds-Barred Beatdown. And at the end of it all, Discord becomes deathly afraid of Spyro and is reduced to begging to be spared. Spyro does so, but only because of Elora telling him that killing the draconequus is not worth it, given that he surrendered.
- Queen Chrysalis and the Changelings - Chrysalis gets ratted out early by Spyro, who detects her dark magic and immediately nullifies her disguise spell. This will lead to her launching her invasion while Spyro and company look for the real Cadence. When she launches her invasion, a good number of the changelings are killed by Spyro's fire, save for Thorax and a few others who side with him. To face Spyro, Chrysalis then turns herself into a doppelganger of him, and is able to match him using her love energy. She also attempts to use this to confuse Spyro's allies, failing only because she says something that Spyro never would, which in turn leads to Spyro and company calling her out for being a terrible actor. But because her energy supply is finite, she eventually runs out of steam. She is then overthrown by Thorax, who steals her remaining love energy and shares it with the surviving Changelings. When she attempts to flee, vowing revenge on Spyro, she gets cut off by the other Dragon-Worlders, who then have her arrested and locked away.
- Alternatively, Thorax and the other rogue changelings share their love energy with Spyro, who then uses a supercharged blast of fire to incinerate the changeling queen. Her ashes are then used as an example for all future villains for what happens to those who cross Jendovahzoor.
- King Sombra - Is killed by Spyro when he is supercharged by the energies of the Crystal Heart, with his horn also being destroyed to prevent his resurrection in The Beginning of the End.
- Plunder Vines - Are incinerated by Spyro's fire.
- The Mane-iac - Is killed when Spyro utterly destroys the rules of the enchanted comic's world with his abilities, which in the comic are Story-Breaker Powers comparable to those of heroes such as Superman or Captain Marvel.
- Tirek - Is fought by adult Spyro in a devastating battle on the same scale as in Dragon War, which ends with him exploding after he attempts to steal Spyro's magic and finds it's too much for him to handle.
- Starlight Glimmer - Is exposed early on during Spyro's visit to her village because he and the other Dragon-Worlders are immune to her Cutie Mark-removing spell. While she was presented as a villain pre-Heel–Face Turn in canon, the Dragon-Worlders won't see her as such, given she's not bent on taking over the world and just wanted to have friends. And when Spyro helps her to see that she shouldn't let her own fears of losing friends rule her life, she joins him and quickly befriends Trixie because of their similar histories with Spyro.
- The Storm King - Arrogantly challenges Spyro after stealing the Princesses' magic, but is unable to beat him because the dragon's power is far greater than that of all the Princesses' combined. Instead of being turned to stone, he is incinerated, with his essence also being wiped from existence to prevent him from returning to life in the future. And to add insult to injury, the remnants of his army, Tempest Shadow, and Grubber soon pledge their loyalties to Spyro in exchange for their survival.
- Alternatively, Spyro roasts(no pun intended) The Storm King for having the demeanor and goals of a jock who "peaked in high school and never got over it," and takes a page from Bane, saying, "When your dream is ashes... then you have my permission to die." He then proceeds to slaughter his soldiers and destroy his zeppelins while the Storm King watches in horror before the purple dragon kills him last. Afterwards, he banishes Tempest Shadow from the land forever lest she be the next to perish by his hand, designating her as a villain in his mind because she helped the Storm King.
- Cozy Glow - Her plans fail when Spyro detects her evil aura early on, which leads to her being more closely monitored by Twilight and company. When she attempts to carry out her plan anyway, Spyro nearly kills her until Elora talks him down from it. However, this brush with death will be so frightening for Cozy that she'll end up going straight and swearing off villainy after the Season 8 arc ends.
- An explanation for her nefarious behavior will also be given in the form of backstory, likely involving something tragic like neglect, abandonment, or abuse by parents or relatives.
- Grogar - Revealed to be Real After All, he then tries to drain Spyro's magic just like Tirek did, but it will prove to be too much for the Bewitching Bell to contain, and the Bell will explode, killing the evil goat.
- Alternatively, he'll be killed by Malefor, who then steals his magic to empower and resurrect himself.
If Chrysalis does survive after A Canterlot Wedding, she will hold a burning hatred not for Starlight Glimmer, but rather Spyro.
Recognizing the immense power that Spyro carries with him and the power of the Elements of Harmony, Chrysalis will seek that power for herself, and will not only create the Mean Six, but also Dark Spyro, whose personality will be very strongly based on that of his Skylanders Academy incarnation.
And just as Spyro's presence has radically altered the events of the show, Dark Spyro's presence in the chapter(s) will lead to many changes in how the story of the episode plays out. For instance:
- Instead of being none the wiser to Chrysalis' creations in the end, the Mane Six quickly catch on when they find each other seemingly acting out of character.
- The encounters that the members of the Mane Six have with their dark counterparts culminates in a Mirror Match where each clone becomes almost a manifestation of the original pony's inner demons.
- Whereas the clones were killed by the Tree of Harmony in the actual episode, they survive in the fic and go on to become recurring villains in subsequent episodes after having cut their ties with Chrysalis.
- Instead of Mean Twilight attempting to lead the clones, Dark Spyro will do so instead, much like how Spyro took Over the Mane Six's mission back in War of the Night.
In this story, the horn in the caves below Canterlot actually belongs to him. Sometime in the ancient past, Malefor came to Equestria with the intent of conquering it and enslaving its inhabitants, only to fall at the hooves of Celestia and Luna. This event was what left Celestia with a strong aversion for Spyro and his fellow Dragon Worlders.
Later on, he resurrects himself by drawing upon the dark magic of some of Equestria's most powerful villains and seeking out his descendant, Spyro. This arc culminates in a showdown with Spyro that ends with the heroic purple dragon banishing him from Equestria. It will also cement Spyro's place as the land's greatest hero and protector.
Contrary to the above, Spike will still find himself asking questions about his origins despite the Great Dragon Migration not passing over Equestria. These unanswered questions then lead to him leaving for the Dragon Lands. In this case, however, the Dragon Worlders follow Spike into the Dragon Lands. Spyro's presence, in turn, will help to show the impact he's had on the world beyond Equestria, as the dragons will now speak to each other in hushed whispers when he's near because they are deathly afraid of him.
Her experience will also leave her with deep gratitude for Spyro and the Dragon-Worlders because she recognizes them as the ones who saved her and her family from dying.
- Alternately, Spyro will follow her after hearing the CMC's complaints about her and Silver Spoon's bullying of them and learn about her home life under Spoiled Rich. Realizing Diamond's bullying tendencies are a result of being abused by her mother, Spyro will scare Spoiled Rich into getting her act together and set Diamond down a better path.
- Alternatively, Spyro lets the other five become Mare-Do-Well, and when Rainbow Dash gets jealous, he'll call her out for having "novice envy" again and drop some sly hints that will get Rainbow Dash to figure out the identities of Mare-Do-Well. Also, after her five friends are unmasked, Mare-Do-Well will return in the same way that Red X did, becoming a recurring character after a pony who isn't one of the Mane Six puts on the costume.
During their time together, Sunset will then befriend Twilight Sparkle because she finds they both don't regard friendship as highly as Celestia does.
- Alternatively, she does escape through the Mirror, but Spyro immediately jumps through in pursuit, just as he had done when he first came to Equestria. Sensing the innate power that Spyro possesses, Sunset will use the crown on herself and achieve her demon form almost immediately when he arrives. This then leads to a fight similar to the one in Man of Steel that levels most of the city while Spyro beats the demon out of her, ridding her of her own inner darkness before bringing her back to Equestria to face judgment for her crimes.
That said, Daring Do will likely find some artifacts in her travels that pertain to this lost history. She will also likely discover an ancient prophecy that foretells of how a purple dragon would defeat evil. These discoveries, in turn, will draw the attention of Spyro and the Dragon Worlders, who will seek her out in order to learn these secrets and help Spyro further pursue his destiny.
This movement will eventually escalate until around the time when Twilight ascends, at which point they will call for Twilight to become Equestria's new ruler as by that point she'll have proven herself to be far more competent and responsible in how she handles problems.
- Her decision to keep the petrified Discord in the Canterlot sculpture garden like some common lawn ornament instead of a safe, secure location away from and unknown to the public where he cannot sense strife and conflict between ponies he can use to free himself.
- Choosing to side with the false Cadence when Twilight starts chewing her out, which Spyro then supplements by cancelling her disguise spell and revealing her true identity.
- Or for deciding to go along with Shining Armor and Cadence's wedding despite knowing Canterlot is under threat instead of postponing the wedding until the threat is neutralized.
- Withholding knowledge of the Crystal Empire and the existence of its former tyrant leader from Twilight
- Also, her withholding knowledge of the hippogriffs until the Storm King's attack.
- Iron Will, who is recruited when Spyro tells him there are other ways he can inspire ponies to stand up for themselves beyond his seminars.
- Double Diamond, Night Glider, Party Favor, and Sugar Belle, who are all recruited when the Dragon Worlders encourage them to share with the world a revised vision of Starlight's equality philosophy that not only embraces their differences, but also encourages ponies to use their talents in the service of others.
- Pharynx, who will be even more stubborn and difficult to reform than in canon. Becoming the Token Evil Teammate in Spyro's group, he'll undergo a multi-chapter character arc that will see him eventually warm up to his allies and respecting Spyro, now seeing why Chrysalis came to regard him as a Worthy Opponent.
- Season 1:
- Look Before You Sleep - Slice of Life
- Bridle Gossip - Slice of Life
- Swarm of the Century - Adventure
- Winter Wrap-Up - Slice of Life
- Call of the Cutie - Slice of Life
- Fall Weather Friends - Slice of Life
- Suited for Success - Slice of Life
- Feeling Pinkie Keen - Slice of Life
- Sonic Rainboom - Slice of Life
- A Dog and Pony Show - Adventure
- Green Isn't Your Color- Slice of Life
- Over a Barrel - Adventure
- A Bird in the Hoof - Slice of Life
- The Cutie Mark Chronicles - Slice of Life
- Owl's Well that Ends Well - Slice of Life
- Party of One - Slice of Life
- The Best Night Ever - Adventure
- Season 2:
- The Return of Harmony - Adventure
- Lesson Zero - Slice of Life
- Luna Eclipsed - Slice of Life
- Sisterhooves Social - Slice of Life
- The Cutie Pox - Slice of Life
- May the Best Pet Win! - Slice of Life
- The Mysterious Mare-Do-Well - Slice of Life
- Sweet and Elite - Slice of Life
- Secret of My Excess - Adventure
- Family Appreciation Day - Slice of Life
- Baby Cakes - Slice of Life
- Hearth's Warming Eve - Slice of Life
- The Last Roundup - Slice of Life
- The Super Cider Squeezy 6000 - Slice of Life
- Read It and Weep - Slice of Life
- Hearts and Hooves Day - Slice of Life
- A Friend in Deed - Slice of Life
- Putting Your Hoof Down - Slice of Life
- It's About Time - Adventure
- Dragon Quest - Adventure
- Hurricane Fluttershy - Slice of Life
- Ponyville Confidential - Slice of Life
- MMMystery on the Friendship Express - Adventure
- A Canterlot Wedding - Adventure
- Sheila befriending Applejack, who will take notice of the kangaroo's powerful kicking strength and recruit her for applebucking on her farm (which could cause for a comical moment where Sheila kicks too hard and accidentally snaps an apple tree in half)
- Sergeant Byrd bonding with Rainbow Dash due to their mutual love for flying
- Bentley connecting with Fluttershy due to being a Gentle Giant despite his hulking exterior.
- Agent 9 striking it up with Pinkie Pie due to them both being eccentric wild cards.
- Rainbow Dash and Ami bonding over their love of racing and competing.
- Tawna and the Nitro Squad befriending Rarity, who notices their beauty and recruits them to serve as models in her boutique, with the Bandicoots donning dresses for new fashion lines of her own design.
- Coco and Twilight bonding over being the smartest of their groups.
- Look Before You Sleep - Spyro ends the tension between Rarity and Applejack and spices up Twilight's sleepover with more video games.
- Bridle Gossip - When Zecora comes to town, Spyro calls out the ponies for being prejudiced and for contradicting themselves by reminding them of how they welcomed him and the other Dragon-Worlders. Also, when the ponies describe the Everfree Forest as being an "unnatural" place, he shuts it down by saying things like "clouds moving by themselves" and "animals taking care of themselves" is exactly how his world works.
- Winter Wrap-Up - Spyro and company use magic to bring Spring to Ponyville, while also showing the ponies that they need to evolve their traditions to accommodate those who are capable of using magic, like Twilight.
- Call of the Cutie - Spyro shows Apple Bloom that she doesn't need to be ashamed of not having a Cutie Mark yet, encouraging her to unlock her potential, thus leading to the creation of the Cutie Mark Crusaders.
- Fall Weather Friends - Spyro gets annoyed with Rainbow and Applejack's competition, hilarity and Dope Slaps ensue.
- Suited for Success - Elora helps Rarity make outfits for not only the ponies, but also for herself and her fellow Dragon-Worlders.
- Feeling Pinkie Keen - Bianca calls out Twilight on her attempts to understand Pinkie's Pinkie Sense and hangs a lampshade on how Twilight cannot accept her friend's "Pinkie Sense" when she herself is able to accept magic in her world.
- Sonic Rainboom - Hunter knocks some sense into Rainbow Dash when she starts panicking about losing in the Young Flyers' Competition.
- Green Isn't Your Color - Elora helps Fluttershy to come clean about not wanting to be a model and later takes her place, helping Rarity start a new fashion line. Also, Spyro gets jealous of all the attention Elora's getting and becomes extremely protective of her.
- A Bird in the Hoof - Elora, who's surprisingly knowledgeable about Philomena's nature, helps her to care for the ailing phoenix.
- The Cutie Mark Chronicles - Instead of hearing stories about how Twilight and friends got their Cutie Marks, the Dragon-Worlders tell the Cutie Mark Crusaders stories of some of their greatest adventures.
- Owl's Well that Ends Well - Spyro calls out Spike for having "novice envy" and tells him to get off his high horse.
- Party of One - Spyro, who's Genre Savvy enough to recognize the episode's "Forgotten Birthday" plot, allows Pinkie to realize the reason why everyone's been avoiding her.
- Lesson Zero - Because Twilight doesn't see friendship in the same light as in canon, she will not have her Freak Out.
- Luna Eclipsed - The Dragon-Worlders call out ALL of Ponyville for insulting Luna, whom they help to adjust to modern life with video games, and she becomes an Adorkable Gamer Chick as a result.