Edwards is accused of illegally using campaign donations to keep his mistress hidden, but Lowell's questions apparently were intended to bolster the defense's argument that Edwards used the money to keep the secret from his wife, not his campaign.
If convicted, Edwards faces up to 30 years in prison.
If Edwards didn't have a strong reaction to his wife's meltdown, he had a much stronger reaction when another of his aides raised questions about his secret relationship with Hunter during Edwards' presidential campaign.
The confrontation with Josh Brumberger took place in a private room at Chicago's O'Hare Airport as Edwards and others were about to take off for a trip to China.
Brumberger said it was a "fairly emotional, heated, somewhat graphic conversation," and Brumberger looked sheepishly at Judge Catherine Eagles and the prosecutor before quoting Edwards.
"What I remember ... 'If he thought I was f***ing her, why didn't he come to me like a man and tell me to stop f***ing her," Brumberger recalled.
"He was really upset. He was red," Brumberger said.
When asked if he was fired, Brumberger replied, "That's the way I understood it. One thing was definitely clear. I was not going to China."
Brumberger's comment drew laughter from the court, which he was able to do repeatedly during the day in a change from the first eight days of the trial that has consisted of often emotional and angry testimony.
Brumberger was 27 when he was part of Edwards staff during the 2007-08 presidential campaign and recalled first meeting Edwards' girlfriend Rielle Hunter when she approached Edwards in the bar of a New York City hotel.
She soon appeared as part of the campaign staff as a videographer, and Brumberger said he looked up on the internet.
"There was a lot of sex, drugs, rock and roll and astrology," Brumberger testified. He said he told Edwards that "Miss Hunter looked a little nutty."
Soon, Hunter was making demands to be allowed at most of Edwards' events and to fly with Edwards on private jets. He noted that Edwards was carrying or wheeling her luggage.
Brumberger remembered being in the Driskell Hotel in Austin, Texas, and seeing Hunter exit an elevator wearing "what I would consider overnight apparel." The elevator did not lead to her room, but it did lead to Edwards' room, he said.
Twice Brumberger said he approached Edwards to warn him that there was a perception problem regarding Hunter. "I felt our relationship to be a bit strained after that," he testified.
When Edwards didn't change his behavior, Brumberger took his concerns to two senior campaign advisers and soon after was summoned to the O'Hare meeting with Edwards.
Brumberger also described the first meeting between Edwards and wealthy philanthropist Rachel "Bunny" Mellon, who agreed to give Edwards more than $700,000 for the coverup effort.
The money came to be known as "Bunny money" by those involved in hiding Hunter.
Brumberger said the meeting at Mellon's home in Haymarket, Va., was remarkable for the luxury.
"It was a beautiful, gigantic property, horse country, rolling hill," he said.
When they left for North Carolina, they left in Mellon's private jet and "we took off from a runway on her property," Brumberger said.
"It was the first and only time in my life I took off in an airplane from someone's front yard," he said.
Mellon liked Edwards and wanted to help him, and Andrew Young later contacted Brumberger, who was traveling with Edwards, reminding Edwards to call Mellon and wish her happy birthday.
The call was obviously successful. After the call, Brumberger sent Andrew Young an email message that read, "Bunny is still in love," which drew laughter in the courtroom.