The 44-year-old comedian joined Melissa Etheridge on Thursday's Watch What Happens Live With Andy Cohen, and chimed in when the singer was asked about a song she'd performed on a previous episode of the show that was presumably about Jolie's divorce from Brad Pitt, though she does not mention the actors by name.
When asked if she'd received any backlash from the song, the 57-year-old singer, who is a friend of Pitt's, answered, "No, it was really tense there for, like, a day. You know, getting threatened. And then it all just, poof, went away."
Handler then quipped, "I did, actually, I heard from both of them. ...I heard from Angelina Jolie and she was like, 'You f**king b**ch.' And I'm like, 'It's not me, it's Melissa Etheridge.'"
Both women have been somewhat vocal about the famous couple, with Etheridge saying in an interview that she stopped speaking to Pitt after he married Jolie. Handler has been more forthright about her dislike of Jolie, making jokes on TV programs and her stand-up comedy shows.
Cohen jokingly pointed out, "This is like a meeting of the Angelina Jolie fan club."
Handler, a longtime friend of Pitt's ex-wife, Jennifer Aniston, admitted that she has some regrets about how she's spoken about Jolie in the past.
"You know what, I'm upset that I was so upset with Angelina Jolie," she confided. "I realize she's just trying to do her best, too."
Handler quickly added, "I mean, obviously, I'm not going to hang out with her, but I get it now. I have more sympathy and empathy for people that are like, 'She's really a mom and a wife and whatever she is. I'm not sure but good luck to her.'"
Back in May 2017, the Life Will Be the Death of Me author appeared on WWHL and was asked what she would do if she was ever to be stuck in an elevator with Jolie.
"I would just look up. Exactly what people do when they're in elevators. You know what you do when you just fake look at the numbers because you don't want to make eye contact," she quipped. "That would be exactly the elevator ride. Then I'd go, 'Heyyy,' as I walked out."
After Jolie and Pitt announced they were divorcing, Handler made quite a few jokes and jabs at their expense. "Brad and Angelina always said they wouldn't get married until everyone could get married," Handler said during an episode of her Netflix show, Chelsea. "And I always said I wouldn't get married until they got divorced. So I'm officially accepting proposals! I'm ready!"
Prior to this slight shade, Handler had slammed Jolie several times. In 2010, she bashed the 43-year-old actress during a foul-mouthed stand-up show in Newark, New Jersey. "[Angelina]'s a homewrecker, she is," she insisted. "She can rescue as many babies from as many countries as she wants to, I don't f**king believe you."
Then, on an episode of WHHL in 2013, Handler went into further detail about why she wasn't a fan of Jolie. "It has nothing to do with Jennifer," she declared, referring to rumors that Jolie and Pitt started seeing each other when he was still married to Aniston. "As a woman, I know when you see somebody walking across the room that's a bad girl. I just don't like Angelina Jolie. I don't think she's a girl's girl. I like girl's girls!"
Here's more on Handler's long-running dislike of Jolie: