Brown, who died of heart failure Christmas morning at 73, lay in repose on the stage where he made his 1956 debut, with the quiet of final respects broken only by the sound of his music.
"The Apollo was always his home because that's where it all started," said his agent, Frank Copsidas, "and the people of Harlem were his family."
Brown lay resplendent in a blue suit, white gloves and silver shoes. Flanking the casket were giant photographs of the singer performing. An arrangement of red flowers on a white background spelled out his nickname: Godfather.
It was maybe the first time the hardest-working man in show business graced a stage in stillness, but that didn't stop his fans from partying.
"This is a celebration of his life," said 41-year-old Bryant Preudhomme of suburban New York. "James Brown gave you heart. He lifted you up when you were down. He gave you hope."
Fans of the late "Godfather of Soul" lined up outside the theater to pay their last respects. Brown's body had been driven from Georgia early Thursday and then taken through New York City's streets for Brown's last date on the historic stage.
At the evening program for family and close friends, the Rev. Al Sharpton said it was difficult to believe that a man who was "so much alive" was dead.
"How could someone with such energy and life really ever be gone?" said Sharpton, a close friend of the Godfather of Soul for three decades.
Sharpton credited Brown with inspiring countless musicians in all genres and with refusing to become a conformist.
"He became a superstar on his own terms ... he never bent, buckled or bowed," Sharpton said. "James Brown wasn't just No. 1, he changed the beat of music all over the world."
Apollo historian Billy Mitchell said Brown routinely drew the largest crowds of anyone at the theater.
The Apollo has been used for public viewings several times before, but always for employees. In 1992, the theater provided a last chance to honor Ralph Cooper, who founded Amateur Night, the weekly talent contest that launched the careers of Brown, Billie Holiday, Sarah Vaughan and Ella Fitzgerald, among scores of others.
The theater also was a showcase for such superstars as Stevie Wonder, Aretha Franklin, Diana Ross and a young Michael Jackson.
Outside on Thursday, its marquee read: "Rest in Peace Apollo Legend The Godfather of Soul James Brown, 1933-2006," and Brown's epic "Live at the Apollo" album streamed from the marquee speakers.
A man taped flowers and pictures of Brown on a wall next to the Apollo, and less than a block away, a merchant showed videos of Brown's live performances on a television outside.
New York City resident Olive Conteh-Martyn recalled children trying to emulate his dance moves when she was a teenager in Sierra Leone, in West Africa.
"We idolized him," she said.
"Brown was as fast as lightning!" said West Webb, who hoped to get into the Apollo on Thursday to pay tribute. "He was one of a kind."
Brown continued to work to the end, dying less than a week before he was to perform New Year's Eve in Manhattan at B.B. King's blues club. Chaka Khan, the Grammy Award-winning rhythm and blues performer, will play instead.
The Associated Press contributed to this report.