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BOSTON — Sometimes the guard changes slowly. Sometimes it changes overnight.

That is what is happening in the city of Boston, which has been led by white men since its incorporation in 1822. With the nomination of Mayor Martin J. Walsh as President-elect Joseph R. Biden Jr.’s labor secretary, the 2021 mayoral race is suddenly wide open, and the front-runners are all women of color.

If Mr. Walsh is confirmed and resigns from his mayoral post, his replacement as acting mayor will be Kim Janey, president of the City Council, a 56-year-old community activist with deep roots in Roxbury, one of Boston’s historically Black neighborhoods. Ms. Janey has not said whether she plans to run.

The two declared challengers in the race are also, for Boston, nontraditional. Michelle Wu, 35, a Taiwanese-American woman, has as a city councilor proposed policies on climate, transportation and housing that have won her the support of progressives.

And Andrea Campbell, 38, a city councilor who grew up in public housing in Roxbury, has drawn on her own painful personal history — her twin brother died of an untreated illness in pretrial custody — to press for policing reforms and equity for Black residents.

Others are expected to jump into the race, but it has already deviated from the long-established pattern in this Democratic city, in which one figure from the white, working-class, pro-union left would hand off power to a similar man of the next generation.

Paul Parara, a radio host who, as Notorious VOG, grills local politicians on his morning show, said Mr. Walsh’s departure cleared a path for long-awaited change.

“I’m ecstatic that Marty is going to Washington,” said Mr. Parara, who works at 87FM, a hip-hop and reggae station. “It does represent an opportunity for Boston to turn the page, and elect someone who looks like what Boston looks like now.”

The percentage of Boston residents who identify as non-Hispanic whites has steadily dropped, to 44.5 percent in 2019 from 80 percent in 1970.

“Oh, we’re about to Georgia Boston,” he added, referring to voter mobilization that has reshaped the politics of that state.

He said he hoped the next mayor would impose greater pressure on police unions, which he said had negotiated advantageous contracts with the city and which, as the Boston Globe has reported, remained more white than the city’s population as a whole.

“I think that’s going to change,” he said. Mr. Walsh, he added, “is a labor guy, and that’s what benefited the police — they were negotiating a contract with a labor guy.”

A new mayor could also rethink development in Boston, where a technology boom and housing shortage have squeezed out poor and middle-income families, or grapple with the city’s egregious wealth inequality: In 2015, the median net worth for white families was almost $250,000, while that figure was $8 for Black families, according to a study from the Federal Reserve Bank of Boston.

Mr. Walsh, who has been mayor since 2014, has responded to progressive activists, but he has also styled himself as a consensus-builder, trying to satisfy a range of stakeholders, including the police and developers.

His successor may, for the first time in the city’s history, emerge from “a left that derives from the civil rights movement, or the residents of color in the city or the left-wing intellectuals in the city,” said David Hopkins, an associate professor of political science at Boston College.

“We don’t have a model of what a different type of mayor would look like because we really haven’t had one,” Mr. Hopkins said. “What’s so interesting about this situation we’re in now is that there isn’t an obvious next Marty Walsh figure in line to take the baton.”

Despite weeks of hints that Mr. Walsh would be tapped as labor secretary, the news of his selection seemed to catch many off guard. The power of incumbency is extraordinary in Boston; the last time a sitting mayor was defeated was in 1949.

So many people were now floating possible runs that Segun Idowu, the executive director of the Black Economic Council of Massachusetts, renamed his Twitter account Not a Boston Mayoral Candidate.

On Saturday, Ms. Wu received a heavyweight endorsement from Senator Elizabeth Warren of Massachusetts, her former professor at Harvard Law School and the person she credits with steering her into politics.

“Bostonians can count on Michelle’s bold, progressive leadership to tackle our biggest challenges, such as recovering from the pandemic, dismantling systemic racism, prioritizing housing justice, revitalizing our transportation infrastructure and addressing the climate crisis,” Ms. Warren said.

But after a year of national soul-searching about race, voters may be drawn to a candidate from the heart of Boston’s Black community, like Ms. Campbell or Ms. Janey.

When she started her campaign in September. Ms. Campbell focused squarely on the city’s history of inequality, noting that “Boston has a reputation as a racist city.”

“I love this city,” she said. “I was born and raised here, as my father was before me. But it’s important to realize that this isn’t just a reputation nationally. It’s a reality locally. Plain and simple, Boston does not work for everyone equitably.”

Progressives should not presume that young voters will turn out for a city election, warned David Paleologos, director of the Suffolk University Political Research Center.

Historically, participation has skewed older and whiter than the city as a whole, with a disproportionate number of votes cast in white, middle-class enclaves like West Roxbury and Hyde Park. Turnout in recent mayoral elections has consistently remained below 40 percent.

The city has changed so much and so rapidly, though, that past experiences may not be an accurate guide.

Mary Anne Marsh, a Democratic strategist, noted that Representative Ayanna Pressley pulled off the biggest political upset in the state’s recent history, ousting a 10-term incumbent and fellow Democrat in 2018, despite being outspent two-to-one.

“Southie is not the old Southie,” Ms. Marsh said, referring to South Boston. “Southie is a lot of young professionals, it’s not South Boston, Irish, Catholic labor families anymore. It is mostly young millennials. It’s a very different place, and that’s true in many pockets of the city. People will be very interested in the race.”