"Debbie Dingell, that's a real beauty," Trump said of the congresswoman, noting he was watching her on television during impeachment proceedings.
Trump said that he gave the family the "A-plus treatment" after John Dingell died, and that the congresswoman, who now holds his seat in the House, told Trump during an emotional call following John Dingell's funeral that her husband would have been "thrilled" by the respect shown for him during his funeral and "he's looking down" on the ceremonies.
"Maybe he's looking up," Trump said, drawing some moans and groans from those in Battle Creek, Michigan, about two hours away from Debbie Dingell's district. "Maybe, but let's assume he's looking down."
Trump's comment about John Dingell, the longest ever serving congressman, fell mostly flat on a crowd in an important swing state that has long revered the former dean of the House. John Dingell was an iconic figure in Michigan who was admired across party lines, and was one of the most popular political figures in the state during his lifetime.
Michigan was key to Trump's election in 2016 and appealing to Midwestern voters like those in the Great Lakes State will be important in his quest to hold onto the White House.
Debbie Dingell responded on Twitter to Trump's attacks on Wednesday, accusing him of sharpening her grief going into the holidays without her husband.
"Mr. President, let's set politics aside," she tweeted. "My husband earned all his accolades after a lifetime of service. I'm preparing for the first holiday season without the man I love. You brought me down in a way you can never imagine and your hurtful words just made my healing much harder."
Dingell's fellow Michigan representative, Republican Rep. Fred Upton, said late Wednesday night that "there was no need to 'dis' him in a crass political way. Most unfortunate and an apology is due."
Appearing on CNN's "New Day" Thursday morning, Debbie Dingell again emphasized her desire to not politicize her husband's death but insisted she wasn't going to let Trump's attacks intimidate her.
"I'm going to keep doing my job," she told CNN's Alisyn Camerota. "If he thinks he's going to keep me from doing my job, I'm going to be right back at it when I leave here."
Asked about Trump's comments on ABC's "Good Morning America" Thursday morning, White House press secretary said she felt sorry for Debbie Dingell's loss, but when asked to explain Trump's attack, she replied, "you'd have to talk to the President about that."
"He was at a political rally," Grisham explained. "He has been under attack and under impeachment attack for the last few months then just under attack politically for the last 2 1/2 years. I think as we all know the President is a counterpuncher."
Trump's rally insults marked the second time in five days that he has mentioned John Dingell's funeral while disparaging the congresswoman, who has supported impeachment.
"The last time I spoke to Debbie Dingell was her call thanking me for granting top memorial and funeral service honors for her then just departed husband, long time Congressman John Dingell," Trump tweeted Saturday. "Now I watch her ripping me as part of the Democrats Impeachment Hoax. Really pathetic!"
Dingell told CNN's Brooke Baldwin on Monday that she was "really hurt" by Trump's tweet.
"It really felt awful, you want to know the truth," she said, her voice becoming briefly emotional. "I'm already missing him."
She added that she hadn't wanted her husband's funeral "to become political."
"I was very grateful for his call, he really did care about my loss," Dingell said of Trump. "And so it really hurt. To say to you that that didn't shake me and didn't bother me would be a lie."
CNN's Nikki Carvajal contributed to this report.