"This is about one thing and that is a failure to uphold expected standards on government documents. It is a very serious mistake, regardless of who the minister is, regardless of personal life," he said.
Couillard had once been involved with a member of a biker gang who was assassinated. She later married a biker gang member but they quickly divorced.
She conceded that neither man had been an innocent but added: "I have done nothing to embarrass my country."
Bernier's resignation spectacularly ends the political career of a man who some believed could eventually challenge for the position of prime minister. It also removes a foreign minister who looked out of his depth from the start.
Bernier had been industry minister when Harper asked him to take over at foreign affairs and sell the Afghan mission to the politically influential French-speaking province of Quebec, where anti-war sentiment is traditionally high.
The new minister made one speech in Quebec on the mission but then disappeared from view over the file, only regaining the spotlight when details of his ties to Couillard came to light.
All three opposition parties blasted Harper for not providing more details about the documents.
"Obviously Mr. Bernier has been suffering from an accumulation of blunders over the past number of weeks. The issue has now come to a breaking point," senior Liberal legislator Ralph Goodale told reporters.
"The prime minister has a lot of explaining to do."
Couillard, who first came to public attention last August when she was pictured in a very revealing dress alongside Bernier, also said President George W. Bush had paid her a compliment at a reception at the United Nations last year.
"Well well well, haven't you been keeping good company," she quoted Bush as telling Bernier.
