Louise Kelton, 57, has been formally sworn into the post, which holds legendary status in the United States.
It is the oldest federal law enforcement office in America and marshals track down some of the country's most wanted fugitives.
Ms Kelton, who moved to Louisiana aged 23, is marshal for the Middle District of Tennessee.
She was born on a US air force base in Wales to an American serviceman and a Welsh mother, and was brought up in the Butetown district of the capital, where her mother and brother still live.
In 1978, she gave up her job as a physiotherapist and moved to Louisiana, where her father was from.
She only intended to stay in the States for year but ended up studying and graduating with honours from Texas Southern University in 1992 with a bachelor's degree in Criminal Justice.
She said: "My dad was an American serviceman and I just wanted to see where he was from.
"Basically my idea was to come over here for a year and bum around and then come back home, but I ran out of money money in Nashville, so I got a job."
Ms Kelton also holds a master's degree in Public Service Management from Cumberland University, Tennessee.
She spent 33 years with the Metro Nashville police department, rising through the ranks from patrol officer through sergeant, lieutenant, captain and finally commander of the city's North Precinct before becoming deputy chief five years ago.
Marshals are also charged with protecting the federal courts and their officers, transporting prisoners and serving arrest warrants.
The role was most famously portrayed by John Wayne and Tommy Lee Jones in Hollywood movies such as True Grit and The Fugitive.
She is only the second black woman to hold the post.
Ms Kelton's mother and brother still live in the Cardiff home she grew up in.
Brother, David Watkins, said: "She's a very high achiever. I've always been proud of my sister. She's my big sister."
Former teacher and family friend Betty Campbell said: "She's made us feel really really proud."
President Barack Obama has nominated a physiotherapist from Cardiff to become a US marshal.