Firedrake the dragon has flown from his new home at the Rim of Heaven in the Himalayan Mountains, to MÍMAMEIÐR, in Norway. MÍMAMEIÐR is a sanctuary for fantastical and mythical creatures run by Firedrake’s friends, the Greenblooms. Barnabas and Vita Greenbloom run the sanctuary with their daughter, Guinevere, and their adopted son, Ben.
Ben is Firedrake’s dragon rider, and the two share a bond so close that they can almost read each other’s thoughts. The past two years have been difficult for them, as they have been apart. The Rim of Heaven is a barren and foreboding valley, high in the mountains — perfect for dragons, but not for humans. Firedrake has been taking care of a revived colony of dragons, and Ben has been helping the Greenblooms with their work. Firedrake has come to MÍMAMEIÐR to say goodbye to his dying dragon friend, Slatebeard.
After Slatebeard turns to stardust, Firedrake prepares to fly home to the Rim of Heaven. However, news from Vita and Guinevere, who are in Greece, delay his plans. They have found that one of the two remaining Pegasi has died of a snake bite. Her mate, Ἀnemos, is beside himself. Vita and Guinevere want to bring their clutch of eggs back to MÍMAMEIÐR to hatch.
Ben and Barnabas begin preparations for taking in the eggs. Twigleg, Ben’s friend, is a homunculus (tiny human). He scours the library for relevant information and is heartbroken to discover that the mother must lick the eggs at the six-week point or they will not grow and the foals inside will die. As Vita and Guinevere, accompanied by Ἀnemos and the eggs, arrive in the sanctuary, Barnabas enlists the help of their conservationist friends from around the world. He learns that the only hope the eggs have to survive is to be treated with a solution made from the sun feather of a griffin.
To retrieve a sun feather is fraught with danger. No one has a clear idea of where the remaining griffins live. And even if they are found, they are known to be very territorial and violent, killing without a second thought. Barnabas tells Ben that griffins consider dragons their mortal enemies. They will fight Firedrake to the death as a matter of honor. To keep Firedrake from harm, they tell the dragon they are only seeking a phoenix feather and will not need his help.
Barnabas, Twigleg and Lola Graytail — the world’s only rat aviatrix — fly to Indonesia in a wooden plane owned by their friend Hothbrodd the troll. Firedrake offers to fly Ben as far as Indonesia on his way back to the Rim of Heaven, giving them the opportunity to spend a little more time together. Sorrel, the brownie that serves Firedrake and who is his constant companion, joins them.
After a long and exhausting flight, Firedrake, Sorrel and Ben land in Indonesia. Firedrake tells Ben that he and his mate, Maia, are expecting their own children. The eggs will hatch in three months’ time. Although good news, it means Firedrake will not be able to visit MÍMAMEIÐR for a very long time. As Firedrake sleeps, Ben decides that once he helps Barnabas obtain the griffin’s sun feather, he will find a way to the Rim of Heaven so he can be with Firedrake, even if he is the only human there.
Once the dragon has rested, they fly to the rendezvous with Barnabas and the others at a temple to Garuda, who is the god of the birds. Firedrake waits a short distance away so as not to alarm the animals. Ben, Barnabas and Twigleg question the many birds worshiping at the temple about the whereabouts of the griffins.
They are led to a female parrot named Me-Rah, who claims to come from the island the griffins inhabit. Poachers captured and sold her, but she escaped. She agrees to guide them to her island and show them the great lion-birds that live there. She warns them, however, that the lion-birds will kill them. Before Ben leaves with Barnabas, Firedrake gives him a locket with one of his scales inside. Should Ben ever need his help, he only has to touch the scale. Firedrake will sense Ben’s need and come.
Me-Rah accompanies Ben and the others aboard Hothbrodd’s plane and tells the story of how she was captured from her beautiful island home. The others glean enough clues to figure out which island, among the thousands that make up Indonesia, is home to the griffins. Hothbrodd lands the plane, and they set up camp. In the dead of night, Ben and Twigleg hear the call of the griffins. It appears that all the tales of them being ferocious creatures are true.
In the morning, Lola and Twigleg set off in her tiny plane to scour the island from the air. Ben and the others start the search on land. After tromping through the forest all morning, they are attacked by a band of primates, including macaques, gibbons and lorises, who take them prisoner and bring them to the secret hideout of a griffin named Shrii. Me-Rah escapes and searches for Twigleg and Lola.
Ben is impressed with the griffin’s immense size — he is about as big as a full-grown dragon. Although Shrii is not violent, he believes Ben and the others are in league with his enemy, Kraa, the griffin ruler of the island. Kraa is violent and cruel, often capturing and selling animals that inhabit the island to poachers for gold.
As if to prove his point, Kraa’s minions, another group of primates, attack Shrii's hiding place. They capture Shrii and take him and his prisoners to Kraa’s stronghold. Along the way, Ben’s locket, which had been taken by one of the macaques serving Shrii, is lost. Ben is heartbroken at losing Firedrake’s gift.
Firedrake senses something is wrong. His mate graciously tells him to find Ben, although she encourages Firedrake to take another dragon along for help. He decides to take a young dragon nicknamed Tattoo because of the beautiful designs of flowers and leaves left on his skin while he had been encased in stone. Tattoo is thrilled to have the opportunity for adventure, even if it includes possible danger. Sorrel, the brownie that serves Firedrake, is not thrilled, but decides to go help Ben, too.
Back in MÍMAMEIÐR, the Pegasus eggs are being looked after by a variety of large fowl. Their father, Ἀnemos, very rarely visits, too afraid of becoming attached to his offspring, only to lose them should Barnabas fail. Guinevere is thrilled to see the eggs become translucent so she can see the foals inside. Ἀnemos begins to have hope that his children will survive as Guinevere says her father seldom fails to keep his promise.
Ben, Barnabas and Hothbrodd are imprisoned in bamboo cages hanging in the trees. Giant scorpions populate the floor beneath the cages. An Indonesian boy, Winston, is also being held prisoner along with his pet tarsier, a tiny monkey with large eyes. Meanwhile, Me-Rah finds Twigleg and Lola and leads them to Shrii’s nest, but it is empty. The following day they meet TerTaWa, a gibbon who serves Shrii. He learns they are friends of the strangers captured with Shrii and offers to lead them to Kraa’s nest.
Kraa accuses Shrii of trying to take over his island. He believes Barnabas, Hothbrodd and Ben were going to help Shrii steal his treasure of gold. Kraa promises to kill all of Shrii’s friends and servants before he kills the griffin himself. As Lola and Twigleg sneak into the nest and try to find some way to help the others escape, they are captured. Kraa decides to sell Ben and his friends to the poachers who frequent the island, before he kills Shrii and his primate followers. Kraa will also trade Winston, as he knows the poachers will give him a lot of gold for the boy because previously he has freed animals they had captured.
Firedrake, Sorrell and Tattoo arrive at the island. Me-Rah finds them and guides them to where the poachers are buying Ben and the others. The dragons chase away the poachers and save their friends. Although grateful for their help, Barnabas encourages the dragons to leave before the griffins see them and want to fight them.
Hothbrodd finally tells Firedrake the truth. They need a griffin’s sun feather in order to save the Pegasi. Firedrake is furious that Ben lied to him. Although they will be outnumbered, seven to two, Firedrake and Tattoo choose to stay and help their friends, even if it means fighting the griffins. Tattoo asks Winston to be his dragon rider and the boy eagerly agrees.
Ben and Barnabas, along with their old and new friends, come up with a plan to steal a sun feather from Kraa while simultaneously freeing Shrii from his cage. Barnabas and Hothbrodd climb up Kraa’s tree, using a dart gun to stun the animals Kraa uses as guards. The primates hurry to free Shrii while Twigleg and Lola sneak up on Kraa. Unfortunately, even though Shrii is freed, Kraa awakes as Twigleg tries to steal his sun feather. Kraa’s screech brings the other six griffins back from their hunting expedition, and one attacks Shrii and the dragons. Tattoo breathes fire on the griffin and it turns to stone and falls to the ground.
Twigleg, now being held by Kraa and his servant, Nakal — a proboscis monkey — tries to convince his captors that the other griffins are rebelling and want to steal Kraa’s gold. Then Kraa hears Firedrake’s roar. He challenges Firedrake to a duel in exchange for the lives of Twigleg, Ben, Barnabas, Shrii and all his followers. But if Firedrake loses, Kraa will eat them all and drink the dragon’s blood so he will become immortal. Firedrake agrees, but only if the prisoners are freed, whether he wins the duel or not, and if they also can take one of Kraa’s sun feathers. As Kraa does not believe he will lose, he agrees to the terms.
A mighty battle ensues, and Firedrake eventually overcomes Kraa. Tattoo, caught up in the violence of the fight, swoops down and lights Kraa on fire, turning him to stone. Shrii is made the new king of the island, but he refuses to rule. He and two other griffins will seek another island to inhabit and rule in peace. Shrii does not have any sun feathers to give to Barnabas, but he insists one of the older griffins gives up their sun feather to pay Kraa’s battle debt. Shrii also gives the griffin his share of Kraa’s treasure for the feather.
Ben had made up his mind to leave MÍMAMEIÐR and live with Firedrake at the Rim of Heaven, but the dragon convinces him to stay with the Greenblooms. Now that Tattoo knows the way, he can bring Ben to visit when Firedrake’s children are born. Ben happily agrees to this arrangement before Firedrake flies back to the Rim of Heaven. Tattoo carries Winston, Ben and the feather to MÍMAMEIÐR while the others fly in Hothbrodd’s airplane. They arrive in time for a potion to be made and the Pegasus' foals to be saved.