Holding back tears as she took the stand at her trial into phone-hacking offences, Brooks said she had been extremely close friends with Coulson, and on occasion had intimate relations with him between 1998 and 2006.
Coulson, who succeeded Brooks to edit the now-defunct News of the World Sunday tabloid from 2003 to 2007, went on to become the spokesman for Prime Minister David Cameron.
He is also on trial with Brooks at the Old Bailey and the prosecution has accused the two former editors of having an affair at the time their staff were hacking into voicemails to secure exclusive stories.
Prosecutor Andrew Edis had told the jury in October when the trial opened that the intimacy of their relationship indicated both knew as much as the other about the criminal activities of senior journalists on the paper.
Brooks said on Friday: "First of all it's not true," of the allegation of an affair but then accepted suggestions from her lawyer Jonathan Laidlaw that they had had moments of intimacy.
"My personal life was a bit of a car crash for many years," she added.
Brooks, the 45-year-old journalist who worked her way up through the ranks from local newspaper researcher to head of Murdoch's British newspaper arm, was almost moved to tears as her lawyer asked her about other former relationships.
At one point, as Laidlaw said he would move on to the topic of Brooks' marriage to actor Ross Kemp and their attempt to have a child, she asked if she could have a break and left the court.
She also revealed that a cousin had acted as a surrogate to help her and her second husband Charlie have a baby, called Scarlett. Charlie Brooks, a friend of the prime minister whom she married in 2009, is also on trial for trying to hide evidence.
The relationship between Brooks and Coulson was discovered after police found a document containing a 2004 letter on a computer at Brooks' London home. She had written the letter after Coulson tried to break off the relationship.
"I do not know if anyone has been in the situation at a time of hurt - you come home and have a couple of glasses of wine and shouldn't go on the computer," she said, adding that she had woken up the next day and thought better of sending the letter.
Brooks was responding to questions as Laidlaw guided her through her career. The former editor, who was a close associate of both Murdoch and Prime Minister Cameron, also told the court on Friday she had not been aware of the tens of thousands of pounds that was paid to private investigator Glenn Mulcaire who has admitted phone-hacking.
Brooks had told the jury of nine women and three men a day earlier that she had not even heard of Mulcaire and that it was impossible for an editor to know every source for every story.
Brooks and Coulson are accused of conspiring to hack into the voicemails of high-profile public figures or those close to them and also of making illegal payments to public officials. They deny the charges.