The commission voted 6-0 to order the repayment after conducting an audit of the campaign.
Edwards' attorneys have said the Democrat's campaign doesn't owe anything. A telephone call by AP to Edwards' attorneys seeking comment was not immediately returned.
Federal auditors said the campaign understated its cash on hand and overstated its expenses, including money spent to wind down the campaign. Auditors also found that the campaign failed to itemize more than $4 million in loan repayments.
Such audits are required by law for federal campaigns that accept public financing, several of the commissioners noted.
"It is not at all unusual for a campaign to have a discrepancy," said Ellen Weintraub, a commissioner. "It's just a math problem and that's how the math worked out."
Federal auditors said about $2 million of the amount to be repaid was attributable to federal matching funds the Edwards campaign received but did not deserve. Auditors said the repayment should include $141,808 in uncashed checks the campaign issued to donors that were never cashed, according to the audit.
The campaign got nearly $13 million in matching funds after it was approved by the Federal Election Commission in December 2007. Edwards dropped out of the race Jan. 30, 2008.
The Federal Election Commission's ruling is the latest problem for Edwards, who was indicted last month on federal charges that he accepted illegal campaign contributions to hide an affair during his unsuccessful 2008 White House bid. Edwards, who was the 2004 vice presidential nominee, has pleaded not guilty to six felony charges that include allegations he filed false campaign reports to cover up the payments.