Maxime Bernier was forced out when it was revealed that he left classified documents at the home of Julie Couillard.
His former girlfriend handed over the papers, believed to be briefing notes for a Nato summit in Romania last month.
The security slip-up was compounded by the fact that Miss Couillard, 38, has had a string of lovers involved with the biker gang and its criminal activities.
Stephen Harper, the country's Conservative prime minister, said he had accepted the resignation of Mr Bernier, 45, following a series of gaffes and embarrassments.
Miss Couillard, a glamorous brunette, was once married to an outlaw biker and lived with another who died in a bloody turf war over drugs in the 1990s.
Mr Harper said he had ousted his foreign minister for the "very serious mistake" of mislaying the documents.
However, his claim that Mr Bernier had not been forced out over his private life came just as Miss Couillard was preparing to go on television.
The former model, who is now an estate agent, came to public attention when she appeared, wearing a low-cut dress, on Mr Bernier's arm during his swearing-in ceremony last August.
Opposition politicians who have been calling for Mr Bernier's resignation stepped up their calls in recent weeks as further details emerged about Miss Couillard.
Between 1993 and 1996, she lived with Gilles Giguere, a Hells Angel lawyer in Montreal.
She was questioned over a murder linked to Giguere but she was released without charge.
Their relationship ended when, following his arrest over a cache of sub-machineguns and marijuana, he became a police informer and was gunned down before he could give evidence.
In 1997, Miss Couillard began seeing and later married Stephane Sirois, an enforcer for the Rockers, a Hells Angels-affiliated biker club.
He also turned informant and testified against a dozen of his former colleagues in a 2002 trial. The couple divorced in 1999.
Miss Couillard, who also runs her own security company and is an aspiring actress, has never been charged with any crime.
However, she was arrested during an investigation into motor-cycle gangs. It also emerged on Monday that she was involved in an attempt by another former boyfriend to provide security at Montreal airport.
Although Robert Pepin never won the contract, his company was provided with information about security at Trudeau International Airport.
Mr Pepin, who committed suicide in 2005, had reportedly received threats over a large sum of money he owed to a Hells Angels loan shark.
Opposition MPs have pointed out that the biker gang has been known to infiltrate organisations to further their activities.
Miss Couillard said on Monday that she had recently discovered that her Montreal home had been bugged. She admitted that her former boyfriends were "not choirboys". However, she insisted that Mr Bernier was "aware of everything". They met last year and, a month after they started dating, he asked her to be his official companion, she said.
She refused to discuss the contents of the papers left in her home but said Mr Bernier was aware he had left them behind after their relationship ended.
Miss Couillard, who claimed that she was "definitely not a biker's chick", said she had once caught the eye of President George W Bush at a reception in New York.
She claimed that Mr Bush glanced at her and jovially told Mr Bernier: "Well, well, well, haven't you been keeping good company."
Mr Bernier had been attacked over a series of political gaffes, including promising aid for Burma on a plane that was not available.
