The show on the seven-candle Hebrew lamp will run simultaneously from May 15 to July 23 at the Vatican museums and the synagogue complex in a city which once housed one of the oldest Jewish communities in the world.
The artifacts are being loaned by nearly 20 museums around the world, including London's National Gallery and the Louvre in Paris.
Among them will be one of the earliest known depictions of a menorah, an engraved stone found at the site in Israel where a synagogue from the Second Temple period was discovered by archaeologists in 2009.
Christian medieval candlesticks inspired by the menorah, as well as the works of contemporary artists, will also be on display.
But history's most precious menorah, made out of solid gold, will be missing.
The candlestick, depicted on the Arch of Titus in Rome, was one of the spoils brought back to the city by the Romans after they sacked the Temple in Jerusalem in 70 AD.
It was initially placed in the Temple of Peace but later disappeared, possibly looted by the Vandals in the sacking of Rome.
Rome's Rabbi Riccardo Di Segni said the unprecedented joint exhibition, more than three years in the making, showed the "evolution in the dialogue between Jews and Catholics".
"Times have changed, many positions have softened," he told AFP.
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