Billie Farrell swam across the Ohio River at age 11, boated on a large reservoir in her home state of Kentucky, and cared for nearly a dozen horses during her childhood in Paducah, about halfway between Nashville and St. Louis.
It was a small-town Southern upbringing for Farrell, far from the salt water that would become as familiar to her as western Kentucky, and far from the wooden decks of the USS Constitution, where in a chilly outdoor ceremony Friday she became the ship’s first female commander in its 224-year history.
“I have been humbled by the outpouring of support I have received as I embark on this amazing journey,” Farrell, 39, said in her remarks.
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It’s a job, she said earlier this week, that demands much more than providing colorful tours for throngs of visitors to the world’s oldest commissioned warship, which is docked in the Charlestown Navy Yard at the end of the Freedom Trail.
It’s also about keeping 80 active-duty officers and sailors in a state of combat readiness, even as they immerse themselves in a 19th-century milieu that evokes the storied history of the undefeated Constitution, the naval hero of the War of 1812 and one of the country’s six original frigates.
“The mission of the Navy today is not that much different from the War of 1812,” Farrell said. “At any point, we could be called to the fight.”
Farrell, who will lead the Constitution for two years, replaced Commander John Benda, a native of Dedham who served four years on the ship, the first two as executive officer.
“What was a fraternity is now a fraternity-sorority,” Benda said with a smile at the USS Constitution Museum during an event preceding the change of command.
Benda told Farrell playfully that his stint as second-in-command gave him an advantage over what the new commander will face on a three-masted, square-rigged, wooden ship.
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“You learn on the job,” Benda said.
Farrell, a veteran of six tours on three other warships, is aware of the learning curve that lies ahead for both her and the crew.
“The mission is to preserve, promote, and protect,” she said. “They have to learn the 1812 Navy, and they also have to learn the 2022 Navy.”
The ship’s crew, about one-third of whom arrive straight from boot camp, will report to the 21st-century fleet when their assignments expire aboard the Constitution. But while they’re aboard Old Ironsides, a nickname from the War of 1812, they will learn how to handle 24-pounder cannons and how to furl and unfurl 2,000-pound sails while moving on yardarms high above deck.
“It takes about 20 people on the yards working to heave those sails. It’s kind of like dead-lifting, and you’re 100 feet in the air standing on an inch-wide wire dangling over the ship,” said Chief Petty Officer Elliott Fabrizio, a Navy spokesman.
“Everything you’re doing up there is a balancing act,” he said. “This is an incredibly taxing enterprise.”
The crew fires a salute at 8 a.m. and sunset each day — using a 40-millimeter round loaded with 200 grams of gunpowder — to coincide with raising and lowering the flag.
The sailors also conduct tours aboard the ship and are assigned to funeral details for veterans — two sailors to each, twice a day — within a 100-mile radius of the Charlestown Navy Yard, Fabrizio said.
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And then there are the training sessions, meetings, and physical demands that the Navy requires of all its service members. A period uniform from the early 19th century does not exempt the sailors from modern-day requirements.
“I think a lot of people think we are just tour guides,” Farrell said.
The Constitution, which retains about 10 percent of its original material, rarely sails under its own power. The first time in 116 years occurred in 1997 to commemorate the 200th anniversary of its launch from Hartt’s shipyard in the North End, and it sailed unassisted again in 2012 to mark two centuries since its victory over HMS Guerriere.
On July Fourth, it’s towed into Boston Harbor for a popular turnaround cruise, and the vessel also leaves the pier for a half-dozen other special events per year. The goal for the missions is to return the frigate to its berth exactly as it left, a high-stakes maneuver considering that the Constitution’s continuing survival is something of a miracle.
The ship has come close to being scrapped, once was considered for target practice, and was moved from the Naval Academy in Annapolis, Md., to Newport, R.I., in 1861 to avoid being damaged by Confederate sympathizers.
But its signature place in American history — the Constitution destroyed or captured 33 opposing vessels — helped stave off its demolition and reinforced the legacies of War of 1812 commanders such as Isaac Hull and William Bainbridge.
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“I definitely feel the presence on board of all those leaders and sailors,” Farrell said, who is scheduled to be in command when the Constitution marks its 225th anniversary in September. “I’ve been in awe of the history we were able to preserve here.”
Farrell said she also is proud to be the ship’s first woman commander, following several career postings where she was the senior female officer. Before arriving in Charlestown, Farrell was executive officer on the USS Vicksburg, a guided-missile cruiser. Previously, she served in a variety of positions across her tours, including navigator, weapons officer, and combat systems officer.
“The important thing to me is to highlight the 70,000 women we have serving today” in the Navy, Farrell said of the Constitution assignment.
Farrell is no stranger to the Boston area. She first visited the Constitution as a high school sophomore in 1998 and had her picture taken at the stern. Farrell later graduated from the Naval Academy, where she met her future husband, Navy Commander Paul Farrell, a Peabody native who is scheduled to retire this year.
The couple have two children, 6 and 3, and live in Charlestown, where their two dogs — Bourbon and Fenway — show the tug of the family’s dual geographical allegiances.
For now, it’s a new challenge for Farrell as she balances a demanding respect for Navy history with the service’s real-time expectations.
“Keeping a 224-year-old ship looking sharp is no easy feat,” she said. “But the ship is in great shape right now. There’s nothing else like it.”
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Brian MacQuarrie can be reached at brian.macquarrie@globe.com.