Barry was survived by his grandmother Polly Lee Harris.
The elder Barry was infamously arrested on drug charges on January 18, 1990, after being videotaped smoking crack in an FBI sting.
Liz Matory, 36, his campaign manager in his run for the Ward 8 seat, said Barry was peaceful and reflective in his final hours.
On Sunday they were rushing to return a truck after gathering his belongings from a Washington apartment where he had been planning to move in. The landlord had apparently decided he didn't want new tenants.
Compounding Barry's frustration, he'd lost the home of his late father recently because of his inability to make rent.
"There's so many things that are broken. There's so much stress on his mind and spirit," she said. "By losing the house, he felt another loss because that was his place that he'd go to remember his dad."
Matory said he had adopted an attitude of healing in recent months. The new apartment, adjacent to Rock Creek Park, was ideal for running along the trail. And he'd made an effort to become sober, she said.
Those close to him saw shades of his father in his ambition and his shortcomings.
"He was a very sage person, a very powerful spirit - he was like a champion that we were all kind of rallying to see him win," Matory said. "He took on the responsibility of everyone without having the foundation and strength to focus first on himself, you know."
She added: "He was very strong. And he was able to handle a lot. And I think he inherited that from his father. But he also inherited the hubris, where he was like 'I can handle this'."
Carl Thomas, a childhood friend who served as Barry's field director in his campaign for the Ward 8 council seat, said he perfectly embodied the spirit of his late parents, the late Effi and Marion Barry.
"Effi was an amazing woman, full of character; Marion was an amazing man full of ambition," he said. "And they made a Christopher who was full of ambition and full of character and carried with him the beauty of his mother and the ills of his father."
Trayon White, the Democratic nominee for the Ward 8 council seat, and a protege of the senior Barry, called Marion Christopher Barry a friend who will be missed.
"Chris was like a brother to me. He cared about the community. He had a lot of things that he wanted to work on to better the community," White said.
White, the younger Barry and a dozen others had run to fill the council vacancy left by Marion Barry's death in November 2014. LaRuby May won that special election. But in the election this year for a full, four-year term to succeed the former mayor, the younger Barry had endorsed White, who prevailed in the Democratic primary.
Christopher Barry had started a construction firm last year, he said in an interview with The Washington Post in the fall. He said he was trying to form a community business enterprise, a minority firm that could compete for city contracts.
White said Barry was on the site of one of his construction projects as late as Saturday.
"Chris is going to be missed by me and others who knew him," White said.
DC Mayor Muriel Bowser memorialised the younger Barry on her Twitter account.
"Let's remember the brightest days! Rest in peace dear Christopher!" she posted, along with a photo of the two of them.
DC Council Chairman Phil Mendelson said he was saddened to hear of Barry's death, putting it in the context of the late mayor's life.
"Christopher Barry's untimely passing is a sad ending to the Marion Barry legacy," he said in a statement. "Christopher never asked for the burden that comes with being part of a famous politician's family. We know he cared deeply about our city - his hometown from birth to death. And that his parents cared deeply for him. My condolences to those whom he is survived."
May said in an interview that "My relationship with Christopher extended before and beyond us being on the ballot."
"One of the things I appreciated about him was his commitment to the people in our community," May said. " As a small business owner Christopher continued the legacy of his father by many times offering job opportunities to people."
Fairley McCaskill, Barry's close friend, said his death was especially tragic because he was working to turn his troubled image around.
Either people thought he was too good, people thought he was the child of a crackhead, people thought he was a waste - people had all types of perceptions of Christopher that were not OK
Barry had brushes with the law, including charges related to an alleged outburst at a DC bank branch last year.
"Chris is someone I grew up with and now he's gone," McCaskill said. "This is surreal. Those who really knew Chris, knew that he marched to his own beat and we loved that about him. He had a big heart," she said. "I think a lot of times he was misunderstood based on how he was portrayed in the media, which our goal was to shift that image and portrayal during his campaign run, and help people to get to know him the way we knew him. He was a one-of-kind type of guy and he will be missed tremendously."
Thomas, who attended Jefferson Junior High with Barry, recalled the pressure Barry faced as his father was rocked by political scandal over the FBI sting.
Thomas said children pelted the young Barry with oranges and crack pipes and taunted him in the schoolyard.
"Either people thought he was too good, people thought he was the child of a crackhead, people thought he was a waste - people had all types of perceptions of Christopher that were not OK," he said. "None of us had to grow up with that."
At times, he said, Barry felt alone in the world.
"No one could really understand what he was going through," Thomas said.