Mr. Bloomberg’s proposal to rezone the area failed amid opposition from Council members and community leaders who said the plan was too generous to developers without ensuring sufficient benefits to the public. Mayor Bill de Blasio, who supports the revised plan, said it linked the construction of big buildings in the area to “real-time improvements in its public transit and public realm.”

Councilman Daniel R. Garodnick, a Democrat who represents the area and was the main sponsor of the bill that was approved on Wednesday, said that the rezoning would allow more intensive development near subway stations, which he described as “certainly the right place to put lots of new density.”

The change could result in more ultra-tall towers like One Vanderbilt, which is going up near Grand Central Terminal and will be nearly as tall as the Empire State Building. When all of the additional development rights have been used in a decade or two, the Chrysler Building could cease to stand out on the Midtown skyline.

Before all of the new towers can sprout, developers must strike deals with the owners of landmark buildings like St. Patrick’s. The cathedral has not made full use of development rights for the block it occupies on Fifth Avenue opposite Rockefeller Center, and can now sell the rest, totaling about 1.1 million square feet.

How much are the so-called air rights worth? The market will decide. But the rezoning calls for the city to collect a tax of at least $61.49 per square foot from the sale of such rights.