[13][14] The Joralemon Street Tunnel opened in January 1908 between Lower Manhattan and a temporary terminus at Borough Hall,[12][15] the first underground subway station in Brooklyn.

[17] The extension opened on May 1, 1908; the first train, an express from Manhattan, left Bowling Green at 1:02 a.m. and entered Atlantic Avenue sixteen minutes later.

[21][29] The Brooklyn Rapid Transit Company (BRT) extended its streetcar lines to the Atlantic Avenue station when the IRT extension opened.

[30] To address overcrowding, in 1909, the New York Public Service Commission proposed lengthening the platforms at stations along the original IRT subway.

[31]: 168  As part of a modification to the IRT's construction contracts made on January 18, 1910, the company was to lengthen station platforms to accommodate ten-car express and six-car local trains.

[31]: 150  Nonetheless, the Atlantic Avenue station was never intended as the permanent terminus of the line, and various proposals for extensions and spurs were put forth.

[37][38] Contracts for the Fourth Avenue Line were awarded on May 22, 1908, for the section between 43rd Street and the Manhattan Bridge, but the Board of Estimate did not approve them until October 29, 1909, when a taxpayer's lawsuit regarding the city's debt was settled.

[50] The tunnel was not opened along with the rest of the Fourth Avenue Line station, since the IRT and BRT could not reach an agreement on splitting maintenance costs.

[57][58] The Cranford Company was contracted to build two sections of the Flatbush Avenue tunnel, extending from Fulton Street to Grand Army Plaza, in mid-1914.

The IRT's architects filed plans in mid-1915 for the construction of a glass structure on the south side of Atlantic Avenue, just outside the station, which was to contain stores.

[26][63] To allow this new service pattern, the Rapid Transit Commission allocated $300,000 in May 1918 for the construction of new track connections at the Times Square, Borough Hall, and Atlantic Avenue stations.

[44]: 180  Construction of the segment of the line under St. Felix Street, including the Atlantic Avenue station, was delayed due to disagreements with the LIRR,[53][59] which did not grant the New York City government an easement until 1915.

[89][90] The New York City Board of Estimate appropriated $362,841 for the lengthening of the platforms at Pacific Street, Atlantic Avenue, and four other stations in January 1926[91][92] and awarded the contract to Charles Meads & Company early the next month.

[96] In February 1928, bids were received by the BOT on a project to remove kiosk subway entrances from the median of Fourth Avenue and to relocate them to the sidewalk to improve safety for transit riders.

[97] As part of a pilot program, the BMT installed silencers on turnstiles at the Fourth Avenue Line's Pacific Street station in August 1930.

[101][102] The BOT announced plans in November 1949 to extend platforms at several IRT stations, including Atlantic Avenue, to accommodate all doors on ten-car trains.

[105] The New York City Transit Authority (NYCTA) announced plans in 1956 to add fluorescent lights throughout the IRT portion of the station.

[107] In August 1961, NYCTA chairman Charles Patterson announced a $2.5 million project to reconfigure the tracks between Nevins Street and Atlantic Avenue, reducing the travel time between the two stations by up to one minute.

[119] The complex was planned to be renovated for $26.6 million, but MTA officials diverted funding for the project in December 1989 to cover a budget shortfall.

[132] Local newspaper Newsday wrote that the station suffered from chipped tiles, missing ceiling sections, and flaking plasterwork and that some of the damage had been painted in an attempt to hide the deterioration.

[137] A joint venture of de Domenico + Partners and Parsons Brinckerhoff was hired to design the project,[138] which included a new LIRR entrance, a new lower mezzanine below the IRT station, and ventilation improvements.

[141] When the renovation began, workers dug two temporary 40-foot-deep (12 m) holes, through which they installed supports measuring 90 feet (27 m) long to carry the weight of the street above.

[151] As part of a pilot program, digital announcement boards, train countdown clocks, and improved intercom systems were installed in the station the same year.

[156] The MTA announced in December 2021 that it would install wide-aisle fare gates for disabled passengers at five subway stations, including Atlantic Avenue–Barclays Center, by mid-2022.

[169]: 32–33  Another passageway between the Eastern Parkway and Brighton Line is present at the south end of the station, which also leads to an exit immediately adjacent to Barclays Center.

[166]: 12–13 The station contains a sculpture by George Trakas, Hook (Archean Reach), Line (Sea House), and Sinker (Mined Swell), which was commissioned as part of the MTA Arts & Design program and installed in 2004.

In designing the sculpture, Trakas had intended to compare the station's role as a train hub with the maritime traffic on the Atlantic and Pacific oceans.

[173] A passageway also leads from the Brighton Line station's upper mezzanine[5]: 4  to the basement of the Williamsburgh Savings Bank Tower,[175] as well as directly to the street within the building.

[142][180]: 4  Despite being listed on the National Register of Historic Places in 1980, the control house fell into decline over the years before being temporarily relocated during the station's 2000s renovation.

[204] On June 25, 1923, eight passengers died and many others were injured when two cars of a train coming from 65th Street Terminal derailed and fell toward Flatbush Avenue.