"Mrs. Brooks personally approved nearly 40,000 pounds for stories" to a senior defense official, Edis said.
The long-awaited trial stems from the revelation in 2011 that employees at the News of the World tabloid eavesdropped on the phone voicemails of celebrities, politicians, crime victims and others in their search for exclusive stories.
The scandal led Murdoch to shut the 168-year-old newspaper and spurred wide-ranging criminal investigations into phone hacking, bribery and other illegal behavior by the nation's newspapers.
It also has rattled the country's media, police and political establishments. Brooks and Coulson once top aides to Murdoch and associates of Prime Minister David Cameron are charged along with six others on a variety of counts related to phone hacking, bribing officials and obstructing justice. All deny the charges.
Edis revealed that four others pleaded guilty before the trial began. Three worked at the News of the World: Greg Miskiw, Neville Thurlbeck and James Weatherup, all former news desk editors.
Private investigator Glenn Mulcaire, who was convicted of phone hacking in 2007, also pleaded guilty earlier this year to three new counts of conspiring to hack phones.
Edis said Mulcaire was paid about 100,000 pounds a year by the newspaper to hack the phones of celebrities, politicians and royals, and sometimes their friends and families.
He said it was "an extraordinary arrangement and one which must have required high-level approval." Thousands of pages of Mulcaire's notes containing details of alleged targets will form a key part of the prosecution case.
Prosecutors say the alleged hacking targets included supermodel Kate Moss, actress Joanna Lumley, royal family member Lord Frederick Windsor and Jamie Lowther-Pinkerton, then private secretary to Prince William and Prince Harry.
Edis said the guilty pleas show "there was a conspiracy which involved a significant number of people and it was quite a substantial conspiracy."
The hacking trial which is not expected to end until Easter 2014 is the first major criminal proceeding spawned by the revelation that the News of the World had hacked the mobile phone voicemails of kidnapped 13-year-old Milly Dowler, who was later found murdered.
Brooks, 45, edited the News of the World from 2000 to 2003 Dowler's phone was hacked in 2002 and went on to edit its sister paper, The Sun, and become chief executive of Murdoch's British newspaper division.
Coulson, 45, edited the News of the World between 2003 and 2007 before becoming communications chief to Cameron until 2011.
Brooks and Coulson face charges of conspiring to intercept communications phone hacking and conspiring to commit misconduct in a public office, which refers to illegal payments to officials.
Edis said the allegations include an accusation that Coulson while at the News of the World conspired with royal editor Clive Goodman to pay a royal police officer for a notebook containing contact details of members of the royal household.
Brooks, he said, paid public officials, including a member of the armed forces and a senior defense official, for information while she was editor of The Sun.
Edis quoted a 2007 letter to Britain's press regulator signed by Brooks in which she said that "no payments are made by The Sun without the written authorization of the editor or the editor of the day."
Former News s of the World managing editor Stuart Kuttner and ex-news editor Ian Edmondson also are charged with phone hacking.
Brooks, her husband Charles Brooks, her former assistant Cheryl Carter, and former News International security chief Mark Hanna are charged with attempting to obstruct the phone hacking investigation in 2011 by withholding documents, computers and other equipment from police.
Photographers have clustered outside the court, known as the Old Bailey, since the trial began on Monday. More than 60 journalists are covering proceedings from the courtroom and an overspill annex.
Edis urged jurors to put aside the copious pre-trial publicity surrounding the case, saying Wednesday the issue they had to consider was a simple one.
"There was phone hacking," he said. "Who knew?"
Brooks, Coulson and the other editors deny knowing about hacking. Edis noted that the News of the World was a Sunday paper, publishing just once a week, so editors should have been familiar with its contents.
"It wasn't 'War and Peace,'" he said. "It wasn't an enormous document.
"What you've got to decide," he told the jury, "is how much did they know about what was going on at their newspaper?"