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A 14-year-old boy, Marcus Damon, an undefeated ultimate fighter (street fighter in the original Japanese version), meets Agumon, who has escaped from DATS, a secret government organization set up to defend the human world from invading wild Digimon. After fighting each other, the two quickly become friends, and through a series of events, are inducted into DATS, where they hope to grow in strength.

Marcus' team-mates include the 14-year-old Thomas H. Norstein, a young prodigy, with his partner Gaomon, and 18-year-old Yoshino "Yoshi" Fujieda who has Lalamon for her partner. As the series progresses, Thomas discovers that Digimon respond to the "darkness" in humans, putting them at odds with monsters who seek to use humanity's own vices to bolster their own power.

The plot thickens with the introduction of Merukimon, one of the rulers (as a member of the Olympus Twelve, Merukimon has a god status in the Digital World), of the Digital World who rules the eastern Digital World and lives in the Infinite Ice Ridge, Biyomon and the human boy Keenan Krier, who serves him along with his partner Falcomon. The DATS team tries to unfold the reason for their hatred of humankind, until it is revealed that the real enemy was Akihiro Kurata, a scientist who led an attack on the Digital World years before that resulted in the death of many Digimon, including Keenan's adoptive mother, Frigimon.

Kurata gained the support of the Japanese government and important businessmen like Thomas' father on his plan to destroy all Digimon in the Digital World, claiming they were a threat to mankind. But this was only a facade to occult his main objective. He harnesses the energy of the Digimon he destroyed to power-up Belphemon, one of the Seven Deadly Digimon/Seven Great Demon Lords, and uses it in his attempt to rule the Human World (and eventually the Digital World), but his ambitions were shattered by the efforts of Marcus and his allies.

Kurata's last act was triggering a bomb which collapsed the frontier between the Human and Digital Worlds, putting both en route on collision, which could have led to the destruction of both realms. The collision was halted by the desperate efforts of BanchoLeomon who ordered Marcus to search for Yggdrasil/King Drasil, the Supreme Ruler and God of the Digital World. When the DATS team finally met King Drasil, they discovered that his decision to deal with the crisis unfolded, was to protect the Digital World by destroying the Human World, as the two worlds could not coexist in the same dimension. To perform this task, he assembled his elite guard, the Royal Knights.

Marcus was confused at first because King Drasil somehow had the appearance of his father, Dr. Spencer Damon, who disappeared in the Digital World years before. But it was revealed that King Drasil took his father's body, and his soul was somehow preserved by BanchoLeomon, who was revealed to be Spencer's partner Digimon. After defeating some of the Royal Knights, the DATS team decided to confront King Drasil himself, who after being expelled from Spencer's body, transformed himself into an all-powerful robotic form determined to destroy the Human World by itself.

However, even when the Royal Knights rebel against King Drasil, it won't give up its goal, attempting to destroy both worlds and create a new world. Using their emotions, Marcus and Agumon finally defeat King Drasil, and the two worlds cease their collision course. Before disappearing, King Drasil brings Spencer back to life and he returns to his family, but the Digimon decide to return to the Digital World to help restore it, and in the end Marcus decides to not part with Agumon and goes with them.

5 years later, Keenan and Kristy, Marcus' sister, go to the same school together. Thomas finally managed to find a cure for his sister's illness and became the youngest scientist to win the Nobel Prize at age 19. Yoshi has joined the police with the remaining DATS members, and Marcus and Agumon have become peacekeepers in the Digital World, breaking up fighting between rival Digimon factions as seen when stopping an argument between a group of Goblimon and Shamanmon.