The Huracán RWD was donated to the Pope by Stefano Domenicali, chairman and chief executive officer of Automobili Lamborghini in November 2017 and was personally autographed by Francis.
All proceeds of the auction will be donated to the Holy Father directly, who will allocate the funds towards diverse projects.
The auto was sold at RM Sotheby's Monte Carlo Grimaldi Forum with all of the proceeds from its $861,575 hammer price going to special causes.
RM Sotheby's described the Lamborghini as being in "as-new condition" having remained in static storage since it was built late previous year.
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The Iraqi city of Nineveh, which was besieged by ISIS, will get £430,000 from the sale, with the aim being to allow displaced Christians to return home.
Pope Francis' Lamborghini Huracan has been finished in the Bianco Monocerus white shade, with contrasting Giallo Tiberino stripes and detailing in homage to the colours of the flag of Vatican City.
The Huracan RWD sits on diamond-finished 20 inch Giano wheels with Nero callipers. The vehicle is capable of hitting 0-100 kmph in 3.4 seconds, and tops out at 320 kmph.
RM Sotheby's had a fantastic headline lot this weekend with a very special Lamborghini Huracan.
The Huracán was presented to Pope Francis by Lamborghini boss Stefano Domenicali at the Vatican.