The film, which had thirteen nominations, also won best director, best actor (Masahiro Motoki), best supporting actor (Tsutomu Yamazaki), best supporting actress (Kimiko Yo) and best screenplay (Kundo Koyama), along with wins for cinematography, lighting, sound and editing.
Released last September by Shochiku, the $3m drama has grossed over $32m at the box office as one of the most successful local films of 2008.
Shochiku widened Departures' extended release this month in the run up to its Oscar bid for best foreign-language film on February 22. US distributor Regent Releasing will open the film theatrically later this year.
Departures previously won best film in Montreal and Palm Springs and a cluster of domestic victories, including top honours at the Kinema Junpo magazine awards, Japan's oldest.
In a unexpected result Tae Kimura won best actress for her role in All Around Us, her first leading role, beating veteran actress Sayuri Yoshinaga (Kabei - Our Mother).
The year's biggest box office hit, Ponyo On The Cliff By The Sea, was awarded best animated film and best music (Joe Hisaishi).
Late director Kon Ichikawa and late actor Ken Ogata, who both passed away in 2008, were given special recognition.
The Dark Knight picked up the prize for best foreign film in a category that included Red Cliff Part 1, No Country For Old Men, The Bucket List and Lust Caution.
Japan Academy Prize Winners:
Best film: Departures
Best director: Yojiro Takita (Departures)
Best actor: Motoki Masahiro (Departures)
Best actress: Tae Kimura (All Around Us)
Best supporting actress: Kimiko Yo (Departures)
Best supporting actor: Tsutomu Yamazaki (Departures)
Best screenplay: Kundo Koyama (Departures)
Best animated film: Ponyo On The Cliff By The Sea
Best foreign film: The Dark Knight
Best music: Ponyo On The Cliff By The Sea
Best cinematography: Departures
Best lighting: Departures
Best art direction: Paco And The Magical Picture Book
Best sound: Departures
Best editing: Departures
Special award from the chairman: Kon Ichikawa, Ken Ogata
Topical award (actor): Kenichi Matsuyama
Topical award (film): Suspect X