Prosecutor Andrew Edis told jurors he was disclosing the affair because it showed they trusted each other a lot and shared at least one secret. "What Mr Coulson knew, Mrs Brooks knew too," he said.
Brooks, Coulson and six other people are now on trial, including Brooks' current husband Charles. Brooks and Coulson are accused of conspiring with others to listen to voicemails and commit misconduct in a public office.
Jurors heard their affair, which began around 1998, was discovered by police through a letter saved on a computer belonging to Brooks. The letter was written by Brooks in February 2004, when Coulson was trying to end the affair, Edis was quoted as saying by BBC.
"The fact is you are my very best friend, I tell you everything, I confide in you, I seek your advice, I love you, care about you, worry about you, we laugh and cry together," she wrote. "In fact without our relationship in my life, I am not sure I will cope."
"But Mrs Brooks and Mr Coulson are charged with conspiracy and, when people are charged with conspiracy, the first question a jury has to answer is how well did they know each other? How much did they trust each other?" he said.
"And the fact that they were in this relationship which was a secret means that they trusted each other quite a lot with at least that secret and that's why we are telling you about it."
The trial focuses on allegations of wrongdoing at the News of the World tabloid before it was closed down in July 2011 after claims that journalists had hacked the mobile phone of murder victim Milly Dowler.
Brooks, 45, who resigned from News International in July 2011, faces five charges spanning over a decade. Coulson, 45, who resigned from his Downing Street post in January 2011, faces three charges in relation to his time as editor of the 'NoW'.
The landmark case is expected to grab high-profile worldwide media attention but the UK judicial system bans any comment on active trials until the verdict has been delivered. Justice Saunders is presiding over the case.
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