As the sombre ceremony began and a bitterly cold wind blew, Carter's flag-draped coffin was carried up the stone steps of the cathedral by a military honour guard after its trip from the Capitol, where his body had lain in state for two days.
Fellow Democratic President Joe Biden will eulogise the 39th president who died on December 29 at the age of 100.
Republican president-elect Donald Trump was among the luminaries at the funeral, before Carter's body is returned to Georgia where Carter was raised as a peanut farmer.
Entering the cathedral with his wife Melania, Trump shook hands with his former vice president Mike Pence, who he had clashed with after Pence refused to go along with his attempts to overturn his 2020 election defeat.
Jimmy Carter's remains will be returned to his native Plains following his funeral in Washington DC. (AP PHOTO)
Trump, who will return to office on January 20, sat next to former president Barack Obama, with whom he chatted as introductory music played.
To Obama's right were Laura and George W Bush and Hillary and Bill Clinton.
Biden and first lady Jill Biden walked hand in hand and took seats in the first row next to Vice President Harris and second gentleman Douglas Emhoff.
Canadian Prime Minister Justin Trudeau, vice president-elect JD Vance and Biden's son Hunter were also among the mourners.
Former vice presidents Al Gore and Pence sat side by side.
Tens of thousands of mourners over the past two days filed through the Rotunda of the US Capitol to pay their respects to Carter, who was president from 1977 to 1981, and was awarded the Nobel Peace Prize in 2002 for his humanitarian work.
Some said they admired the former Southern Baptist Sunday school teacher who played a key role in the negotiation of the 1979 Egypt-Israel peace treaty as a gentle man, rather than a partisan combatant.
"We've come so far from where Jimmy Carter was as a person and it's kinda sad," said Dorian DeHaan, 67, who travelled 440km from Sugar Loaf, New York, to pay her respects.
"I hope that this will be a reminder to people of what we need to get back to -- that it's not about the power, it's about the people."
As she waited in the public viewing line outside the Capitol, DeHaan said her daughter married into the family of the president's younger sister Ruth, presenting the opportunity to meet the former president in Plains, Georgia.
"But it's a sad moment," DeHaan said.
"It's the end of an era and I think we kind of have lost this real belief in humanity, in our presidency."
The National Cathedral has hosted the state funerals of Carter's immediate predecessor Gerald Ford and successor Ronald Reagan.
Carter attended both men's funerals and gave the eulogy for Ford, joking that they shared a love of a New Yorker magazine cartoon that depicted a little boy looking up at his father, saying, "Daddy, when I grow up, I want to be a former president".
Following the state funeral, Carter's remains will be returned to his native Plains where he lived in his 44 post-White House years and made the base of operations for his diplomatic work and charitable efforts including Habitat for Humanity.
Carter lived longer than any other US president and had been in hospice care for nearly two years before his death.
His last public appearance was at wife Rosalynn's funeral in November 2023, where he used a wheelchair and appeared frail.
In August, his grandson Jason Carter said Carter was looking forward to casting a ballot for Harris in the November 5 election, which she lost to Trump.
Biden, during his long career in the US Senate, was the first member of that chamber to endorse Carter for president.
