The apology comes almost 150 years after the end of slavery in the country's overseas colonies, which included Suriname and islands like Curacao and Aruba in the Caribbean and Indonesia in the East, where the Dutch East India Company was based in the 17th century.
"Today on behalf of the Dutch government, I apologize for the past actions of the Dutch state," Rutte said in a speech in The Hague.
"We, living in the here and now, can only recognize and condemn slavery in the clearest terms as a crime against humanity," he said.
Dutch ministers have travelled to seven former colonies in South America and the Caribbean for the event.
Sigrid Kaag, the Dutch finance minister and deputy prime minister, said on an official visit to Suriname last week that a "process" would begin leading up to "another incredibly important moment on July 1 next year."
Descendants of Dutch slavery will then celebrate 150 years of liberation from slavery in an annual celebration called "Keti Koti" (Breaking the Chains) in Surinamese.
But the plan has caused controversy, with groups and some of the affected countries criticising the move as rushed, and saying the lack of consultation by the Netherlands smacked of a colonial attitude.
But Rutte in his speech on Monday said that choosing the right moment was a "complicated matter."
"There is not one right time for everyone, not one right word for everyone, not one right place for everyone," he said.
The Dutch funded their "Golden Age" of empire and culture in the 16th and 17th centuries by shipping around 600,000 Africans as part of the slave trade, mostly to South America and the Caribbean.
In recent years, the Netherlands has been grappling with the fact that its Rembrandt and Vermeer-filled museums and historic towns were largely built on the back of that brutality.
The Black Lives Matter movement in the U.S. spurred questions about racism in Dutch society with the cities of Amsterdam, Rotterdam, The Hague and Utrecht formally apologizing for the slave trade.
Rutte had long resisted, previously saying the period of slavery was too far back and that an apology would ignite tensions in a country where the far right remains strong.
He has now changed tack, but that has not pleased everyone.
Sint Maarten's Prime Minister Silveria Jacobs told Dutch media on Saturday the island would not accept a Dutch apology if made on Monday.
"Let me be clear that we won't accept an apology until our advisory committee has discussed it and we as a country discussed it," she said.
The fact that another Dutch minister sent to Suriname, Franc Weerwind, is himself of Surinamese descent sparked criticism.
On Monday, Dutch cabinet ministers would be in Suriname, Bonaire, Sint Maarten, Aruba, Curacao, Saba and St. Eustatius to "discuss the cabinet response and its significance on location with those present," the government said.