The exhibition is called Vermeer and the Masters of Genre Painting.
It gathers a third of the 17th-century Dutch painter's canvasses for the show. They will hang alongside nearly 60 painting by his friends, rivals and contemporaries.
"We wanted to do away with the stereotype of Vermeer as 'the Sphinx of Delft'," said Blaise Ducos, who is in charge of the Louvre museum's vast collection of Dutch and Flemish paintings.
Despite his reputation as one of the greatest painters of the Dutch Golden Age, Vermeer was all but forgotten after his death in 1675.
His reputation was only revived in the late 19th century.
With so little known about the enigmatic painter who died in poverty, it was assumed that he worked alone at his home in Delft.
All but one of his 34 known works are set within its four walls, from the Girl with a Pearl Earring to The Music Lesson, giving the impression, said Ducos, that Vermeer rarely ventured out.
But "Holland at that time was like New York", Ducos told the AFP news agency, an artistic, banking and trading powerhouse, where painters competed for the patronage of its rich merchants.
Vermeer stole and borrowed from his peers including Gerrit Dou, Gerard ter Borch, Jan Steen and Gabriel Metsu, Ducos insisted, all of whose work is featured in the show.
"Vermeer and his contemporaries constantly tried to surpass each other's work in technical prowess and aesthetic appeal," said Adriaan Waiboer, of the National Gallery of Ireland, which has also been working on the show for six years.
"Their creative rivalry contributed to the exceptionally high quality of their work," he added.
While the Girl with a Pearl Earring will not be leaving its home in The Hague, Vermeer's other great iconic work, The Milkmaid, has been loaned to the Louvre for show, which will later travel to Dublin and Washington DC.
The painting, known as the Mona Lisa of the North, is regarded as a symbol of the Dutch nation, and beyond the Netherlands "has a huge place in the collective consciousness", Ducos argued.
The Dutch Republic into which Vermeer was born was the richest country in the world, he added, the birthplace of modern capitalism, its vast wealth built on a powerful navy and its booming East India Company.
It also produced an unprecedented artistic flowering, with artists led by Rembrandt and Frans Hals producing a staggering five million works in the newly independent Netherlands over the course of the 17th century.