Beverly Hills-based Julien's Auctions will offer the dress at an auction on November 17 in Los Angeles as part of a wider Monroe sale between November 17 and 19.
The late fund manager Martin Zweig bought the dress in 1999 for $1.26m at a Christie's auction and has come from his estate. Zweig, who kept the gown in a climate-controlled display case mounted on a mannequin, died three years ago.
French-born, Hollywood costume designer Jean Louis designed the sequin-covered dress that was the same colour as her skin to give the illusion she wasn’t wearing anything once she shed her fur coat to make an entrance at the gala fundraiser for the Democratic Party.
It was said to be so tight that Monroe, star of films including Some Like it Hot and Gentlemen Prefer Blondes, had to be sewn into it.
Monroe's breathless rendition of the song was to mark Kennedy's 45th birthday, which was a couple of weeks after the gala at Madison Square Garden in New York. Monroe died of a drug overdose less than three months after her appearance and the president was assassinated the following year.
"Equivalent of a Monet"
Darren Julien, president and chief executive of Julien's Auctions, said: "It's like the equivalent of a Monet, just because of its historic significance and its connection to one of the most important actresses of our time.”
Monroe would have been 90 years old this year.