Lag gave the name "Niche" to a girl that was a letter whose delivery slip was incomplete and couldn't be delivered, and started taking her to her destination. Lag is enchanted with her hair while he escorts her, and on his way after dropping her off, he learns from some passersby that her destination was actually a freak-show, advertising a new attraction: A child who received the blood of the legendary creature "Maka."

Lag and Niche run after Nelli to get their crossing pass back, however Nelli is found out as an impostor and is going to be punished! Lag and Niche come up to save Nelli, but just then the letter Nelli's late brother Nello wrote to Jiggy Pepper flies away. Lag stretches out his arm with all his might trying to save the letter, and suddenly a shindan flies out from his hand!

Lag, having glimpsed into Gauche's heart, comes to know about his dream to be chosen for the highest title the Bee's that work in the capital can obtain, Head Bee, and that he will soon be transferred there, a first step toward that dream. Nearing the end of their journey, one day before reaching their destination Lag and Gauche get in a fight after Lag asks Gauche to take him with him to the capital so he can search for his mother. Angry, Lag takes off with Gauche's shindanjuu and hurries along by himself, but wanders into Gaichuu territory without realizing it and falls into a trap.

One day Lag Seeing finds himself shipped. His mother abducted by someone, he's now just a package sent by her to be delivered to a friend's house. Gauche Suede is a Letter Bee, a member of the Amberground national postal service, who is tasked with delivering this "letter," together with his partner Roda. The still young Lag rebels at Gauche's seemingly emotionless focus on his work, his heart still reeling from being torn from his mother, but as they head into a valley they are attacked by a ferocious creature known as a Gaichuu.

Lag decides to make Niche his dingo officially, and reaches the Yuusari Head Post Office, known as the Bee-Hive. He and another boy named Macky Gee begin the Bee suitability interview examination, which consists of delivering one real letter safely to its destination. Knowing he is delivering a real letter, Lag's determination is strengthened yet again.

Lag, as well as Niche and Steak, a strange animal that tags along with Niche, reaches the town of Kyrie where the bridge Bifrost connects to Yuusari. There they meet Nelli, who guides them to an inn to stay the night, and volunteers to take Lag's bag up to his room, but then suddenly disappears. Nelli's aim is actually to get Lag's crossing pass into Yuusari.

Some years after he met Gauche, Lag heads to the main post office in Yuusari to take the interview to become a Letter Bee after passing the preliminary examination. After saying all his goodbyes to the people he loves, he heads to the train station with a Letter Bee named Connor that came to pick him up. But when he arrives, he discovers a small girl hiding herself in a small crevice. And what's more, she's a letter, just like Lag was!

Lag goes once again to see Sylvette, alone in her house, and his heart is struck when he sees her crying on the veranda. Lag shoots a shindan from his own body into the shindanjuu Gauche left behind, the Nocturne Op. 20 Shindan Custom, and he, along with Sylvette, learn what was in Gauche's heart. The memories in Gauche's shindanjuu are...

Gauche is no longer a Bee. When Lag heard this from the Bee examination proctor Zazie, he's shocked and depressed. Lag, Nice, and Steak go to see Sylvette, Gauche's sister, but are mistaken for debt collectors and met by a stern, wheelchair bound girl who points a gun at them.

On the morning of the first day of work for new Letter Bee, Lag Seeing, and his dingo Niche, the sub-master of the Bee-Hive, Aria Link, stops by Sylvette's house where Lag is now living. She shows him to a place known as the Hill of Prayer, where everything with Gauche had its beginnings.

Lag begins his daily life as a Letter Bee, and one day goes to pick up a letter from a young man named Vincent Alcott. He has been unsuccessful in fulfilling his dream of becoming an author and in order not to worry his mother back in his hometown, he writes letters filled with lies about his success. When Lag finds out about this, he worries whether such a "letter of lies" really holds any heart.

Aria and Niche final make it to Houdai's house. Aria tries to hand over the letter right away, but is injured when Houdai suddenly attacks her. But Aria doesn't flinch, and tries to convince him by talking about how a person dear to her lost something important on the Day of Flicker. Houdai hears this, lets them into his house, and begins to tell the story of his memories of the incident that happened on board that airship. At around the same time, Dr. Thunderland is treating Lag and Gauche, and the unthinkable occurs...

To stop Lawrence's plan and protect the ones who were unable to become spirit, Noir heads to the Bread and Weapon's Shop, Sinners. Noir asks Jacob, who is surprised to see him and worried, to give him a shindanjuu, and when he leaves the shop he runs into Sylvette. Sylvette is deeply worried, but pretends like she doesn't notice the changes in her brother. Noir is tugged back by those memories of Sylvette, but...

200 years ago, Niche and her twin sister were shunned as cursed, and were eventually disposed of. Thrown into a river, with the most precious thing in the world, her sister, split apart from her, she matured all on her own, and has lived together with the Maka ever since. When Niche finally encounters her, she has no recollection of what happened, and instead protects Lag, a "human." Shocked by seeing her sister in such a state, she tries to kill both her sister and the other people. Lag tries to stop her, and shoots a shindan into her with his feelings...

Ann and Hunt are grabbed by the gaichuu. While Zazie and Connor struggle desperately to attack it, Lag lets loose a shindan that finally catches the gaichuu. His strength exhausted, Hunt falls toward the ground. Hunt, hit with Lag's shindan, projects an image of Sarah and Hunt's cruel past as Gauche and Roda fight to protect the two from a gaichuu.

A therapy relaxation room planned out by Thunderland Jr. has opened up in the Bee-Hive. Lag and Connor are curious and drag along Zazie to go check it out right away. The caretaker for the rest and relaxation room, Mana Jones, lost her sight in an accident, but she has an amazing sense of smell and is a plant specialist. Mana heard about Lag from Gauche in the past, and begins to tell him about what happened during the accident and why Gauche and Dr. Thunderland Jr. are the ones who enabled her to continue her work.

Sylvette receives a fan letter addressed to her from a girl named M. Croce, asking her to make a doll that looks like her to give to her brother who will be leaving his hometown to work in a coal mine shortly. The doll maker, Sylvette, hurries to make the doll, and after spending all night, heads out the next morning to deliver it. Lag is worried and goes with her, but the two of them are tired and end up falling asleep on the rhino carriage!

One day, a trio calling themselves the "Letter Pigeons" barge into the Bee-Hive and challenge the Bees to a race, in order to make a name for themselves and start a letter delivery service besides the Letter Bees. Master Largo thinks it sounds like fun so Lag, Zazie, and Connor take on the Letter Pigeons in a fierce delivery battle!

Lag and Niche are riding a carriage on the way back from a delivery, and the two other passengers are a passionate couple named Bonny and Moss. They've promised to marry each other, but Frank and his gang, who's proposal was rejected, are chasing after them. Niche, after hearing that eloping means getting to be together with the one you love, drives away Frank so Bonny and Moss can be happy together, but the real reason Frank was chasing them turns out to be something else...

Lag delivers a fan letter to the popular pianist Mathilda Rein from a passionate fan of hers named Joey, and learns that she always enjoys reading his letters. But by accident he finds out that those letters are actually written by a different person...

After the effect of being shot with Lag's letter bullet, Noir has awakened back as Gauche Suede. Lag asks Largo and Thunderland Jr. to allow Gauche to go home to the waiting Sylvette, and somehow gets permission for it. However, Largo and Thunderland Jr. can't help but shake off a certain feeling...

Zazie comes back after having lost important letters, and he's injured, too. As the rumor goes around that Zazie threw away the letters in order to escape from the gaichuu, another Letter Bee is to be dispatched from the Bee-Hive to recover the letters and finish the delivery. Lag jumps in to volunteer, but it seems that Zazie braved a dangerous route spotted with gaichuu territories.

"Get away from here"... The boy Lugh works together with an old man he calls "Grandpa" in an imagery lighthouse built out in the wilderness, but he keeps hearing voices from somewhere. Around the same time, Jiggy Pepper is passing by the area on a delivery, and notices that a Gaichuu, Korona, has made a nest on top of the imagery lighthouse. Riding his "iron horse" up the imagery lighthouse, Jiggy Pepper's shindan Lapis Lazuli explodes!

Lag gets a fever. Sylvette and Niche are worried and try nursing him back to health, but Niche isn't used to it and makes mistake after mistake. And whether it's on an errand or shopping she keeps getting distracted as well. Sylvette takes care of them one after another, but Niche dislikes how Sylvette is always nagging her.

Two inspectors from the capital, Akatsuki, come to the Bee Hive. Caribs Garrard and his dingo, Hazle Valentine. They came to investigate a string of letter robberies happening to the south. During one of them, Moc Sullivan is attacked, and the letters he was carrying fall into a ravine. Garrard suspects that there's someone on the inside for Reverse, since they know so much about the Letter Bee's routes and movements, so he forbids them from going to the south. However, one of the letters Moc was carrying was a letter from a sick girl that Lag dictated for her...

A person spotted Noir up in the northern reaches of Yodaka. Lag is ordered by the Bee-Hive Master Largo Lloyd to find out what Noir is up to, and he heads there with Niche and Steak. There he discovers a shell of what looks like a giant gaichuu, as well as a used cartridge which Noir left behind. Lag shoots his own shindan into the cartridge!

The fight between Lag and Noir continues, and Zazie comes back to help after sending Wasiolka to report. Just then a ton of swarming type gaichuu, Lao-Lao, come to attack. Lag and Zazie do their best to fight the gaichuu, but the huge numbers and lack of dingos to back them up makes it a tough battle. But then a trusty ally appears, and finally it's time for Lag to shoot that Letter Bullet!

The Letter Bees are requested by the government to go after the Cabernet, as they still consider it a serious threat. With not enough personnel, the Sub Master of the Bee Hive and now office worker, Aria Link, heads out on a delivery herself. The letter is addressed to a Houdai Franklin, who was on the airship during the Day of Flicker and experienced that terrible accident. Since it's her first delivery in a long while, Niche tags along as her dingo, but the new duo has a tough time working together.

Gauche hurries to deliver a letter from Dr. Thunderland Jr. to Dr. Whitman, the foremost authority on vegetation and herbal research, asking him for a recommendation in order to prove the value of Mana Jones's research to the council. However Dr. Whitman lives far away, and there is not enough time to make it there and back within the given deadline. Even so, Gauche takes on the nearly impossible task...

Niche thinks she has failed at being Lag's dingo, so she runs away from home with her pet(?) Steak. Worried, Lag and Connor head out to search for Niche. However Niche, hungry and wandering aimlessly around town, sneaks into the bread and weapons shop Sinners and tries to finally cook Steak, but the Gobenis catch her in the act.