But prior to Thursday's tweet, Trump had been publicly cordial with Wintour, who is the editor of Vogue, which like Vanity Fair is owned by Conde Nast.
Carter became Trump's nemesis even before he took over Vanity Fair 25 years ago.
The two-time presidential candidate was mocked in a Vanity Fair video that presented the former First Lady with several potential pastimes for the New Year-none of which included seeking office again.
Trump went on to add that Anna Wintour was "a big fundraiser" for Clinton and had been "all set" to be ambassador to the Court of St. James's (the formal title used in the United Kingdom for the American ambassador).
- democracy diva (@democracydiva) December 28, 2017 I hope Anna Wintour responds to Trump. It was there that Carter dubbed Trump a "short-fingered vulgarian", an insult that has followed the president to this day.
The Vanity fair crew said the former Secretary of State would do well to try knitting.More news: Winston Reid benched as West Ham draw with Bournemouth
Vanity Fair's political vertical The Hive is being slammed after the site posted a video in which staff talk about Hillary Clinton.
With the tweet, which was sent while he was at Trump International Golf Club in Palm Beach County, Florida, the president waded into a controversy that existed largely online - and might well have been flickering out.
Commenters were quick to denounce as "sexist" the suggestion of writer Maya Kosoff that Clinton "take up a new hobby in the new year".
For the president, the uproar provided an opportunity to take a dig at two of his favorite targets: Clinton and Vanity Fair.
- Jess Dweck (@TheDweck)Anna Wintour is the artistic director of Condé Nast, but that's for every publication under their publishing umbrella. She is the Queen of being unbothered!
In the video, which Vanity Fair said was meant to be amusing, the editors offered Clinton suggestions on new hobbies that would prohibit her from running for president again, like taking up knitting or volunteering. Also, remember how your wife was on the cover of that magazine at the start of this year? In his defense, the man's brain is essentially beef casserole at this point.