The timescale of the relationship was important in considering if they both knew about the hacking of schoolgirl Milly Dowler's phone and the voicemail from home secretary David Blunkett to Spectator publisher Kimberly Quinn, the Old Bailey trial heard.
Resuming his closing speech, prosecutor Andrew Edis QC turned to the letter of February 2004 in which Brooks declared she had been waiting six years for Coulson, saying she confided in him.
Mr Edis said the letter which was never sent was "at odds" with what both defendants said in their evidence. He told the jury: "Mr Coulson told you soon after this letter in 2004 they got back together again and it carried on until he left the paper in January 2007 which is not at all what Mrs Brooks told you, so you have to decide.
"Why does it matter? It matters for two reasons. One - at the time of the Milly Dowler hacking were they in the sort of relationship that would involve them sharing work-related confidences with each other without inhibition? Secondly, were they back together again by August 2004 so that the same thing applies. Why does that matter? That is the Blunkett hacking. It is not the case to make you think any worse of either of them. Were they at daggers drawn...or were they in fact very close."
While conspiring to commit misconduct in public office was different from phone hacking, in Brooks's case, if guilty of the one charge, it would demonstrate a willingness to "allow your journalists to commit crimes in order to get stories", the prosecutor asserted.
All seven defendants deny the charges against them.
NotW reporter Dan Evans said he played Coulson a hacked message from Sienna Miller to Daniel Craig signing off "I love you" in 2005 but Coulson disputed it.
By April 2006, Mulcaire was "hacked out". Mr Edis said: "At this stage Mr Mulcaire was being tasked... to hack all sorts of people." That included Coulson and Brooks, he said, adding: "So they are turning in on each other."
The trial continues.