WASHINGTON — The Department of Transportation opened a program on Tuesday that allows cities to apply for federal funding to make public transit stations more accessible to disabled people, moving on the anniversary of the Americans With Disabilities Act to provide access to $1.75 billion to update stations that do not comply with the law.

The program, approved as part of the infrastructure law enacted last year, would address a persistent problem in New York and other major cities across the nation that built transit systems long before the A.D.A. was signed into law. The 1990 statute protects people with disabilities from discrimination in public transportation and mandates that they have equal access to transit systems, but many stations constructed before it existed are largely inaccessible to those who use wheelchairs or have limited mobility.

The federal money, $343 million of which will be available this year, will allow recipient cities to renovate subway stations so people who need an elevator, ramp or visual and audible aids can access rail systems.

“It’s one thing to push transit agencies to become compliant; it’s another to fund them and help them actually get done,” Pete Buttigieg, the secretary of transportation, said in an interview to promote the start of the transit program.

Mr. Buttigieg said there were about 900 stations across the country that were not A.D.A. compliant. The department moved quickly to launch the program amid growing concern about inflation, which has raised the cost of renovation projects substantially, he said, but has yet to set a date for when the first round of funding will be disbursed.

The need is particularly great in New York, which has the most noncompliant stations in the country, and where only a little more than a quarter of stations comply with the law. The Metropolitan Transportation Authority recently vowed to make most of its subways accessible by 2055 as part of a settlement agreement in two class-action lawsuits.

“At a time when public transit is depressed compared with prepandemic levels, we need to be as inclusive as possible,” said Danny Pearlstein, a spokesman for Riders Alliance, a New York City-based transportation accessibility organization.

Other cities including Boston and Chicago face similar problems, according to the Department of Transportation.

More than 25 million Americans had a travel-limiting disability, and 3.6 million did not leave their homes because of them in 2018, according to data from the Bureau of Transportation Statistics. The Federal Transit Administration said a quarter of the nation’s rail stations remain inaccessible as of 2020, a Transportation Department representative said.

“I’m just sick and tired of hearing stories of friends or constituents unable to use public transit because they have the nerve to get around in a wheelchair,” said Senator Tammy Duckworth, Democrat of Illinois, a double amputee and the first disabled woman elected to Congress, who led the effort to include the program in the infrastructure measure.

The program, which will ultimately grant a total of $1.75 billion over the next five years, is opening at a time when transit agencies have been battered by drops in revenue from the pandemic. It is a small piece of the infrastructure law, which administration officials, economists and business groups have called the most significant step in a generation toward upgrading critical infrastructure systems in the United States.

Mitch Landrieu, a senior adviser to President Biden who is leading the implementation of the infrastructure law, said the program was in keeping with the administration’s main priority in rolling out its funding: equity.

“Accessibility should never be a barrier,” Mr. Landrieu said. “The impact of accessibility improvements goes beyond people with disabilities because it also makes stations better for parents with strollers.”

When the A.D.A. was enacted 32 years ago, only 6 percent of Chicago’s rail stations were compliant. Now, about 70 percent of its stations have been updated, but the remainder face technical and financial challenges, the Chicago Transit Authority said in a statement.

“Some were never designed to hold an elevator or other accessibility structure. Others are located on either small pieces of land or in the median of expressways,” the statement read. “Rehabbing those stations takes considerable time and money.”

In Philadelphia, renovating older stations will cost roughly $4 billion, according to Kelly Greene, a spokeswoman for the Southeastern Pennsylvania Transportation Authority. SEPTA has created a schedule for making its stations A.D.A. accessible, which includes projects that could be funded by the new program.

Jinny Kim, the director of the Disability Rights Program at Legal Aid, said the program would help prioritize accessibility even as transit systems have dealt with lower rider fares throughout the pandemic.

“People with disabilities can continue to ride transit because they do depend on it,” she said. “When public transit systems are inaccessible, they just can’t access society.”