With Ogiue as new president and several of the original members already graduated, four new members join the society: Ohno's friend Susanna, the loud Rika Yoshitake, the grumpy Mirei Yajima and the mysterious Hato Kenjirou. The new members join the club attracted by Ogiue's yaoi drawings. She welcomes the new members but fears the club will become a "rotten girl" (fujoshi) haven for yaoi fans and that is getting a bit too far removed from its original purpose.

Hato has a difficult time with Yajima and Yoshitake's obsession over his crossdressing. Keiko Sasahara, Kanji's kogal sister, appears in the club's room while Madarame is in there thinking about Saki Kasukabe. Ogiue recruits Genshiken members as employees to help in her manga artist work.

After Madarame lends a thankful Hato his place to change into girl's clothes, both start to become good friends. The group continues their work helping Ogiue finish the club's doujinshi for the Summer Comifes.

Angela returns to Japan to visit the Summer Comifes and do some cosplay with Ohno like she does every year. Two girls from Ogiue's past make an unexpected visit to the club's booth, much to Susanna's chagrin.

In the final day of the Summer Comifes, Angela's sudden and vocal interest in Madarame make him and the rest of the Genshiken have an utterly embarrassing moment. However, Hato's timely confession to the group may be even more shocking than that.

The group has to deal with the aftermath of Hato's confession and its embarrassing (but hilarious) effects on Madarame, Kuchiki and the rest of the Genshiken. A relative of Yoshitake visits the club's room to know more about the University and the otaku society.

Ogiue plans to make a romance manga story for the club's magazine that is going to be published at the Campus Festival, so she asks the members of Genshiken about their past relationships during High School for inspiration. Hato reveals the full extent of his artistic skills and the strange condition that limits them.

Hato talks with Madarame at his apartment to apologize for his actions during the last Comifes. The members of the otaku society struggle to complete their manga stories for the club's magazine.

The Genshiken members successfully participate in the Campus Festival activities, but several different persons from Hato's High School days make an unexpected appearance at the University.

Hato comes to terms with his past and finally reveals the true reasons for his crossdressing. Saki Kasukabe arrives at the Campus Festival just in time to discover Madarame and Susanna in a compromising position.

In the epilogue of Hato's revelation another situation ensues. Madarame and Saki are tricked to be reunited alone in the club's room by Sasahara and a dubious Hato.

After a long and emotional struggle Madarame finally has confessed his feelings to Saki (sort of). Both new and old members of the Genshiken support their fellow otaku friend in the only way they know. Ohno's angst about her future with Tanaka and life after graduation make her cosplay to an extreme.

The Genshiken club members travel together to a spa resort. By using her own personal experiences as an example, president Ogiue gives a troubled Hato some important lessons about love, friendship and mutual understanding.