A story of hope amid squalor in Mumbai, India, Slumdog Millionaire also had wins that include adapted screenplay, cinematography, editing and both music Oscars, score and song.
Director Boyle offered warm gratitude to the people of Mumbai, saying they "dwarf even this guy" as he held up his Oscar statue.
The other top winners: Kate Winslet, best actress for the Holocaust-themed drama The Reader; Sean Penn, best actor for the title role of Milk; Heath Ledger, supporting actor for The Dark Knight; and Penelope Cruz, supporting actress for Vicky Cristina Barcelona.
Sean Penn has his second best-actor Academy Award with his win in the title role of Milk.
Penn's first words upon taking the stage to accept his prize for playing the slain gay-rights pioneer were: "You commie, homo-loving sons of guns."
Slumdog composer A.R. Rahman, a dual Oscar winner for the score and song, said the movie was about "optimism and the power of hope."
"All my life, I've had a choice of hate and love. I chose love, and I'm here," Rahman said.
The epic love story The Curious Case of Benjamin Button, which led with 13 nominations, had three wins, for visual effects, art direction and makeup.
The Dark Knight had a second win, for sound editing.
Man on Wire, James Marsh's examination of tight-rope walker Philippe Petit's dazzling stroll between the towers of the World Trade Center in 1974, was chosen as best documentary.
The supporting-acting categories were presented by five past winners of the same awards. Cruz's award was delivered by last year's winner, Tilda Swinton, plus Eva Marie Saint, Anjelica Huston, Whoopi Goldberg and Goldie Hawn. Ledger's was presented by Kevin Kline, Alan Arkin, Joel Grey, Cuba Gooding Jr. and Christopher Walken.
It was a much different style for the Oscars as each past recipient offered personal tributes to one of the nominees, without clips of the nominated performances. Awards usually are done in chit-chat style between a couple of celebrity presenters.
After last year's Oscars delivered their worst TV ratings ever, producers this time aimed to liven up the show with some surprises and new ways of presenting awards. Rather than hiring a comedian such as past hosts Jon Stewart or Chris Rock, the producers went with actor and song-and-dance man Hugh Jackman, who has been host of Broadway's Tony Awards.
Instead of the usual standup routine, Jackman did an engaging musical number to open the show, saluting nominated films with a clever tribute.
Offering a nod to Slumdog Millionaire, Jackman crooned, "Just a humble slumdog, sitting in a chair, of a millionaire ..."
He hauled best-actress nominee Anne Hathaway on-stage to stand in as Richard Nixon in a gag tune about fellow best-picture nominee Frost/Nixon and asked the question in song - why don't comic-book movies get nominated? - a dig at Oscar voters' best-picture snub of The Dark Knight.
It was something of an inside joke, since Jackman himself has starred in the X-Men comic-book adaptations and this summer's Wolverine spinoff.
Jackman later did a medley staged by his Australia director Baz Luhrmann with such performers as Beyonce Knowles and High School Musical stars Vanessa Hudgens and Zac Efron.
Slumdog Millionaire went into the evening with 10 nominations and an unstoppable run of prizes from earlier film honours.
The film nearly got lost in the shuffle as Warner Bros. folded its art-house banner, Warner Independent, which had been slated to distribute "Slumdog Millionaire." It was rescued from the direct-to-video scrap heap when Fox Searchlight stepped in to release the film.
Complete list of winners
BEST PICTURE: "Slumdog Millionaire" (Fox Searchlight) A Celador Films Production, Christian Colson, producer
LEAD ACTOR: Sean Penn in "Milk" (Focus Features)
LEAD ACTRESS: Kate Winslet in "The Reader" (The Weinstein Company)
DIRECTOR: Danny Boyle for "Slumdog Millionaire" (Fox Searchlight)
FOREIGN LANGUAGE FILM: "Departures" - Japan (Regent Releasing) A Departures Film Partners production
SUPPORTING ACTOR: Heath Ledger in "The Dark Knight" (Warner Bros)
SUPPORTING ACTRESS: Penelope Cruz in "Vicky Cristina Barcelona" (The Weinstein Company)
ORIGINAL SCREENPLAY: Dustin Lance Black for "Milk" (Focus Features)
ADAPTED SCREENPLAY: Simon Beaufoy for "Slumdog Millionaire" (Fox Searchlight)
ANIMATED FEATURE: Andrew Stanton for "WALL-E" (Walt Disney)
ANIMATED SHORT FILM: Kunio Kato for "La Maison en Petits Cubes" (A Robot Communications Production)
ART DIRECTION: Donald Graham Burt for art direction and Victor J. Zolfo for set decoration on "The Curious Case of Benjamin Button" (Paramount and Warner Bros)
COSTUME DESIGN: Michael O'Connor for "The Duchess" (Paramount Vantage, Pathe and BBC Films)
MAKEUP: Greg Cannom for "The Curious Case of Benjamin Button" (Paramount and Warner Bros)
CINEMATOGRAPHY: Anthony Dod Mantle for "Slumdog Millionaire" (Fox Searchlight)
LIVE ACTION SHORT FIRM: Jochen Alexander Freydank for "Spielzeugland (Toyland)", a Mephisto Film production
DOCUMENTARY FEATURE: James Marsh and Simon Chinn for "Man on Wire" (Magnolia Pictures) A Wall to Wall production
DOCUMENTARY SHORT: Megan Mylan for "Smile Pinki", a Principle production
VISUAL EFFECTS: Eric Barba, Steve Preeg, Burt Dalton and Craig Barron for "The Curious Case of Benjamin Button" (Paramount and Warner
Bros)
SOUND EDITING: Richard King for "The Dark Knight" (Warner Bros)
SOUND MIXING: Ian Tapp, Richard Pryke and Resul Pookutty for "Slumdog Millionaire" (Fox Searchlight)
FILM EDITING: Chris Dickens for "Slumdog Millionaire" (Fox Searchlight)
ORIGINAL SCORE: A.R. Rahman for "Slumdog Millionaire" (Fox Searchlight)
ORIGINAL SONG: "Jai Ho" from "Slumdog Millionaire" (Fox Searchlight), music by A.R. Rahman, lyrics by Gulzar
