月島仁兵衞懷着對蟲奉行所的嚮往來到了江户。迷路的仁兵衞得到了果子屋的阿春的接待，兩人在前往蟲奉行所的路上遇到了伏擊人類的蜘蛛，仁兵衞將其擊退。後來蜘蛛趁人不備劫走了小春。仁兵衞和蟲奉行所的三人救出了小春，眾人將巢穴中的蜘蛛一掃而空之後遇到了巨形蜘蛛。無涯先生出現消滅了怪獸，仁兵衞的能力被大家所認可並加入了蟲奉行所。

仁兵衞的目標是超越父親。晨會上松之原向仁兵衞解釋了蟲奉行所的由來，同時也告訴他一年來加入蟲奉行所的新人都沒能堅持下去，仁兵衞被要求一個月內不能拔刀。仁兵衞和火缽在巡邏時交流了過去的經歷，仁兵衞對於無涯先生也有了更多的瞭解。兩人在河邊發現了被襲擊的人類和動物，隨後巨大的青鬼蜻蜓出現了。仁兵衞在戰鬥中救了火缽一命，兩人合力消滅了怪獸蜻蜓。

仁兵衞想要拜戀川春菊為師學習刀法。兩人一同上屆巡邏時遇到了聲討春菊的行人，原來最近出現了刀法強的竊賊。當晚仁兵衞遇到了出現在劫案現場的春菊，為了給春菊洗脱罪名，仁兵衞幫助春菊越獄，兩人準備尋找真兇。松之原向蟲奉行大人彙報了春菊的生平。仁兵衞二人在擺脱警衞追擊時遇到了襲來的大刀螳螂，兩人合力消滅了怪物，原來怪物就是劫案的真兇。

仁兵衞等人合力消滅了進攻街道的蟲子後，一乃谷因為不滿其餘人的表現而脱離隊伍。晚上，一乃谷卻因為害怕蜈蚣而被仁兵衞發現。為了不讓別人發現他軟弱的一面仁兵衞幫一乃谷保守了這個秘密，同時為了克服這個弱點兩人進行了針對蟲子的特訓。次日眾人在街道上遇到了巨大的蜈蚣蟲子，一乃谷為了消滅怪獸保護街道克服了自己心中的恐懼，協助眾人消滅了蜈蚣怪獸。

無涯先生指明要仁兵衞陪同自己前去完成任務。兩人來到了任務指明的地點，接受了委託後兩人查看了蟲子襲擊的場所。仁兵衞消滅了一隻蟲子後眾人遇到了大量的大人蚤，無涯出手將其全部消滅。為了消滅出現在兩個地方的成年蟲子兩人兵分兩路。無涯將蟲子全部消滅後趕到了仁兵衞處，他被仁兵衞頑強的精神所感動。任務完成後兩人回到了蟲奉行所。

潛入蟲奉行所的面具男被仁兵衞和火缽制住，仁兵衞將其帶到了松之原處進行問話。原來他是為了獲取蟲類的知識而來，被揭下面具後長福丸露出了絕美的面容。仁兵衞送長福丸回家時遇到了襲擊人類的夜深蚊，長福丸用艾蒿的煙驅逐了夜深蚊，仁兵衞趁機消滅了怪獸。眾人為了慶祝大醉一場，長福丸趁機潛入，發現了一張秘密的圖卷。松之原要求他保密，否則就要揭穿他的身份。

富士山附近出現了神秘的巨形蟲類。江户城中，蟲奉行所的準備去觀看花火。巨形的獨角仙蟲類襲擊了江户城，除了仁兵衞之外的三人擊退了怪獸的第一波攻擊後準備疏散羣眾，無涯單獨前往討伐蟲類。此時仁兵衞也在蟲奉行所中遇到了神秘的銀髮少女。無涯經過一番苦戰擊退了巨蟲，仁兵衞和神秘少女也找到了合適的觀賞地點觀賞煙花，少女為了感謝仁兵衞送給了他自己的鈴鐺。

蟲狩的成員打算通過蟲奉行所打聽蟲奉行所在的“離”的位置。此時在江户的仁兵衞在休息時路遇了偽裝成受傷少女的蟲狩成員蜜月，蜜月想要通過誘惑仁兵衞探出蟲奉行所的情報。沒有成功的蜜月綁架了阿春威脅仁兵衞，即使如此也沒有探出情報的蜜月和仁兵衞在地底大戰一場。最後仁兵衞帶着阿春在蟲奉行所等人的幫助下逃出了生天。

蟲狩一行人發現了蟲奉行的所在之處並前往進行復仇。為了保護蟲奉行大人蟲奉行所的眾人全軍出動前往八丈島。在海上，眾人遇到了末那蚤的襲擊。春菊和末那蚤大戰一場之後勝利。眾人分開後逐個登島，仁兵衞和火缽在飛行時被蟲狩擊落。仁兵衞見到了蟲奉行，蟲奉行與趕來的蟲狩進行了戰鬥，剩餘的春菊等人也與蟲狩開始了遭遇戰。仁兵衞拼命的保護着蟲奉行。

春菊受到蟲狩挑撥對無涯拔刀相向，兩人開始了鏖戰。仁兵衞仍然在保護蟲奉行，但仁兵衞很快被蟲狩所打倒。另外一邊無涯為了化解春菊的憤怒故意不還手使得春菊明白了自己不是他的仇人。蟲奉行因為仁兵衞的傷而憤怒，變身成為黑鳳蝶將蟲狩三人擊退，但蟲狩使用特殊武器將其打回原形。無涯等人趕到後救出了蟲奉行和仁兵衞，但是兩人撤退時遭到了伏擊。

Cornered by Sougan, the strongest of the Insect Hunters, attacks the Insect Magistrate but seconds before death an unfamiliar Jinbei awakens.

Returning to Edo, the Insect squad is stunned to see mounds of bug carcasses and one man standing alone.

Osono the journalist plans to write an expose about the Insect Magistrates and knows she will get her big scoop at the women's bath.

A new half insect half man has appeared in Edo looking for a certain young samurai. As conventional weapons fail to stop him it is up to Jinbei to test his new skills.

Sanada Yukimura's 10 Crucifix Insects attack one village after another. The Insect Magistrate rushes to Edo Castle, where she discovers a secret in Nagatomimaru's room.

The Insect Magistrate heads to Kishuu to recover her lost powers. Oooka Tadasuke, Edo's smartest man, accompanies her as her guard. Jinbei goes as well, but Oooka is upset by his failings as a Samurai.

Jinbei is chased and captured by the people of Kishuu at the order of Sanada Yukimura. The village of Iwamatsu, where he is kept, is attacked by bandits, and he wins the hearts of the people by chasing them off. However, there is only a brief moment of rest.

Jinbei heads to meet the lord of Kishuu, but he finds Hibachi instead. The party meets with the rest of the City Patrol group and enjoys a brief rest. But the time limit is drawing nigh, and just when the Ten Crucifix Insects attack the people of Kishuu...

The battle with the Ten Crucifix Insects begins! The first round is Tsukishima Jinbei vs. Nedzu Jinpachi. As soon a the battle begins Jinbei is drawn into the castle moat, and forced to fight underwater at a huge disadvantage.

The second battle of Wakayama Castle is against Kirigakure Saizou, the strongest of the Ten Crucifix Insects, who is a master of strange techniques. Hibachi is dazzled and bewildered by illusions of her past.

The Miyoshi brothers have powerful regenerative capabilities. They say that taking life is offering salvation, and in them Shungiku sees his own younger self. Oooka, who knows the old Shungiku, is doubtful he can win the battle.

The fourth battle of Wakayama Castle is between Ichinotani Tenma and Anayama Kosuke. Anayama says "Justice" a lot. He attacks Tenma with his warped sense of justice. A badly wounded Tenma continues to fight, hoping for just one thing: to meet the father and mother he's never seen.

Jinbei's flower team advances steadily. Meanwhile the snow team, the Magistrate's party, reaches the eternal well. Kirigakure Saizou then reveals his true self and begins a one on one fight with Mugai.

The battle for Wakayama castle continues! Muagi battles Saizou while the rest of the Magistrate's fights the last of the crucifix insects, and Jinbei attacks Yukimura. The Magistrate plunges herself into the Eternal Well, and her mysterious past is revealed.

When he learns that the power of the well will cost the servant her memories, Jinbei goes into the well after her. She was prepared to lose her memories but Jinbei persuades her not to. When she leaves, Sanada Yukimura is there...

The well gives the Magistrate back her power and she transforms into Shiroageha, but her memories are lost. She attacks Jinbei, and the power of the well makes Sanada much stronger. Jinbei, who swore to fight until he dies, is faced with his last enemy. The final battle begins!