The iconic white dress fetched $5.5 million (£3.4 million) at the Profiles in History sale and became the most expensive Monroe auction item ever.
It smashed the previous record of $1.26 million (GBP790,000), which the gown the tragic actress wore for her Happy Birthday Mr. President performance fetched.
The item also became the most prized movie costume ever - Audrey Hepburn's little black dress from Breakfast at Tiffany's previously held that honour when it sold for $923,187 (GBP577,000) in 2006.
The Seven Year Itch 'subway' gown was among the items being sold from veteran actress Debbie Reynolds' collection of movie clothing.
Other highlights at the first of two Reynolds Collection auctions included Monroe's red sequin number from Gentlemen Prefer Blondes, which sold for $1.2 million (£750,000), the actress' saloon costume from River of No Return ($510,000/£318,000), Judy Garland's blue cotton dress from The Wizard of Oz, Charlie Chaplin's hat and Dame Elizabeth Taylor's riding outfit from National Velvet.
In total, the auction brought in $22.8 million (GBP14.25 million), which stunned Reynolds.
She tells WENN, "I'm thrilled beyond words. This first auction shows that our great stars were loved by the world."
A second auction of costumes and memorabilia will be held in December (11). Monroe's dress from Bus Stop will be among the items going under the hammer.