Akamaru is a male nin-dog from Konohagakure's Inuzuka clan, serving as the partner, best friend, and constant companion of Kiba Inuzuka. He was entrusted to Kiba by his mother, Tsume Inuzuka, while Kiba was still a student at the Ninja Academy. Their first meeting was memorable, as Akamaru almost immediately urinated on Kiba's face, much to the amusement of Kiba's mother and sister. Despite this inauspicious beginning, the two quickly became inseparable.

Akamaru has a personality that is described as active and devoted. This is most evident in his interactions with Kiba, with whom he spends nearly all his time. They often run through forests together, chasing one another, and in battle, Akamaru's loyalty is unmistakable; he will rush to Kiba's side the moment he is hurt. Beyond this, Akamaru possesses a humorous and somewhat scientific thought process, from his perspective, he has been shown to think humans focus on finding a mate at the wrong times when they should be concentrating on their duties as ninja. He is also very overprotective of Kiba, once trying to pull his master away from a woman he was attracted to, as he did not want Kiba to be distracted from his training. Akamaru does not speak human language like some other nin-dogs, but Kiba can understand everything he communicates through barks.

Akamaru's primary motivation is his unwavering loyalty to Kiba. He is driven to support his partner in all endeavors, from daily training to life-threatening missions. This bond is the core of his existence, and his actions are always focused on protecting Kiba and ensuring their success as a team. In the Sasuke Recovery Mission, for instance, Akamaru bit Kiba's hand to convince him to use a risky, powerful technique when they were losing a fight, showing that his motivation includes pushing Kiba to be his best.

In the story, Akamaru plays a crucial role as a combat partner and a tracking asset. During the Chunin Exams, he helped Kiba cheat on the written test and fought alongside him against Naruto Uzumaki. In the preliminary round, he used the Beast Human Clone technique to transform into a copy of Kiba, causing confusion. He can also ingest a soldier pill, a ninja tool, which temporarily turns his white fur red, amplifies his chakra, and increases his size and ferocity; this is the origin of his name, which means red perfection. During the mission to retrieve Sasuke Uchiha, Akamaru and Kiba developed combination techniques such as Dynamic Marking, where Akamaru urinates on a target with great accuracy to track it by scent, and the Human Beast Combination Transformation: Double-Headed Wolf, where they fuse into a large, two-headed wolf to perform devastating spinning attacks. He was severely wounded in this mission protecting Kiba.

After a three-year gap, Akamaru has grown from a small puppy that could ride on Kiba's head into a massive, horse-sized dog capable of carrying Kiba on his back. Kiba, having spent every day with him, initially failed to notice this dramatic growth. In this period, he and Kiba developed a Three-Headed Wolf technique. During the Fourth Great Shinobi War, Akamaru was deployed with the Allied Shinobi Forces, fighting against White Zetsu army clones and later facing reincarnated enemies from the Sound Village.

Akamaru's key relationships are centered on his bond with Kiba. He is also a member of Team Kurenai, alongside Hinata Hyuga and Shino Aburame, and works well with them as a tracking unit. He has a relationship with Kiba's mother, Tsume, and his older sister, Hana, who is a veterinarian that has treated his injuries. By the end of the original story, many years later, Akamaru has grown old, appearing with wrinkles and spending most of his time napping. He has also sired offspring, including a son named Akemaru who resembles his father's earlier form.