The England and Manchester United striker and his celebrity wife owe the money in the form of commission payments to Proactive, a sports management company who agreed lucrative sponsorship deals with major companies on their behalf, it is alleged.
The firm got commission of up to 20% on multimillion-pound contracts signed by the Rooneys to endorse firms such as Nike and Coca-Cola, Manchester Mercantile Court heard.
But the firms' "primary point of contact" to the couple was Paul Stretford, the footballer's long-standing agent and a former director of Proactive.
But when he left the firm in acrimony in October 2008 he refused to authorise further payments of commission, now worth £4.3 million, forcing Proactive to sue the Rooneys, the court heard.
Mr Stretford signed-up to represent Rooney, then aged under 18, and with the agreement of his parents, in 2002 as the talented youngster burst on to the football scene with Everton, his home town club.
He subsequently signed for Manchester United in a £20 million deal and he and his wife have become household names.
Ian Mill QC, acting for Proactive, opened the complex case against the Rooney's and Mr Stretford at the court today.
"If one believes the quotes attributed in the press," he said, "It appears Mr and Mrs Rooney regard these charges against them as exploitative and financially driven, these are the quotations that appear in a number of national newspapers.
"If by financially driven they mean the claimant wishes to recover the substantial sums due to it, I would respectfully agree, but it is hardly a ground for complaint or for criticism.
"We simply don't understand how this can be their view."
Mr Mill said for almost six years, from July 2002, Paul Stretford, through Proactive had acted for Wayne Rooney "with great success".
The footballer himself was quoted as saying he could not "speak highly enough" of his agent who always got him the best deals.
Mr Stretford looked after transfer dealings and his "off-field" business interests. He also represented Coleen Rooney, helping secure her deals including her TV show, Real Women, a regular column in Closer magazine and sponsorships from Asda and Diet Coke, he said.
But, Mr Mill said, such success must be "equally attributed" to Proactive, for enabling the deals to happen.
However the relationship between Proactive and Mr Stretford broke down over his involvement in a trial at Warrington Crown Court in October 2004 which had an "unhappy conclusion".
The case involved Mr Stretford allegedly being threatened by "certain individuals" when Wayne Rooney left one firm to sign-up with Mr Stretford.
But Mr Stretford's evidence was called into question when the Crown Prosecution Service dropped the case because they could "not rely" on him as a witness.
The Football Association (FA) then brought disciplinary hearings against Mr Stretford over breaches of the Fifa Players' Agents Regulations and FA Rules relating to his acquisition of the right to represent Wayne Rooney in 2002-03 and "false and mis-leading" testimony.
When the board of Proactive refused to financially back Mr Stretford's appeal against the FA the pair parted company on acrimonious terms in October 2008; Proactive claims he was dismissed for gross misconduct, Mr Stretford maintains he terminated his own contract.
He was subsequently banned by the FA from acting as a football agent for nine months starting on May 4 2009.
From October 8 2008 Mr Stretford has refused to authorise payments of commission, said to be due to Proactive from contracts signed by the Rooneys while with Proactive - amounting to £4.3 million over the last 15 months.
Instead Mr Stretford has "constructed a series of absurd and unmeritorious defences".
"Where, I ask rhetorically, is the exploitation?" Mr Mill added.
"I would respectfully suggest if there is any exploitation it's the exploitation of the Rooneys by Mr Stretford who has used them to further his dispute with Proactive.
"In short, Proactive simply seeks the monies to which it is contractually entitled."
The case in Manchester is scheduled to last three weeks with the Rooneys expected to give evidence next week.
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