A site was selected in a residential area at the northwest corner of the intersection of Monroe Place and Pierrepont Street in what is presently the Brooklyn Heights Historic District. The location is the highest point in Brooklyn Heights and was once known as Clover Hill. During the Revolutionary War American troops began to build an earthen fort on the spot as part of the defenses of Brooklyn. After the American evacuation of Long Island, the fort fell into the hands of the British, who redesigned and completed it during their occupation of New York. "Brooklyn Fort" mounted 18 cannon and was 450 feet square with walls that rose 45 feet above a 20-foot deep ditch. When peace came, the fort reverted to the possession of the farmers on whose land it stood. Over the next 50 years they dismantled it as best they could but parts of the ramparts and ditch were visible until 1836 when the present streets were put through and houses and a church occupied the corner.

Construction began on March 1, 1937, and the new courthouse was completed and officially opened on September 28, 1938, at a cost slightly exceeding $1,500,000. Although there were no formal opening ceremonies, the event was marked by the presence on the bench of all eight of the then Justices of the court, making it the only known occasion in which the court has sat en banc.

The court's third home was designed by the Brooklyn architectural firm of Slee & Bryson. The building is of a classical revival style that flourished in the Great Depression and is three stories high, clad in white limestone with a pink granite base. Two fluted Doric columns stand at either side of the bronze entrance doorway and the ornamental grillwork over the lobby windows. A stepped parapet and four bas-relief, sculptural rondels at the third floor adorn the Monroe Place facade. The low height and restrained classical details of the courthouse allow it to harmonize with the nineteenth century buildings in the surrounding historic district.

The interior of the courthouse is also finished in the classical revival style. The imposing lobby has a coffered, vaulted ceiling that is supported by four green marble Ionic columns. There is extensive decorative bronze work on the doors, elevators, railings, and vents. The two-story courtroom is half-paneled in American walnut with acoustical stone from the level of the second floor to the coffered ceiling, which is accented with gold leaf. Four large bronze chandeliers light the room. The clerk's office, administrative offices, and lawyers' lounge complete the first floor. The lounge is notable for its collection of photographs of the Justices who have made up the bench of the court since its founding in 1896. The second and third floors contain nine walnut-paneled chambers for Justices, the court's library, and its consultation room. Hallways throughout the building have marble wainscoting and cork flooring.

When the present courthouse opened in 1938, a complement of 8 Justices and 63 staff were employed in the building, a total of 71. Today at full complement 22 Justices and more than 200 staff serve the court. Present staffing thus represents more than three times the number for which the building was originally designed. And while formerly all of the Justices of the Appellate Division had their principal chambers in the courthouse, currently less than a handful of associate justices and the Presiding Justice have their principal chambers there. The remaining associate justices have their principal chambers in the counties from which they were elected. To further reduce overcrowding, in 1997, the Court’s Law Department was moved to ancillary accommodations nearby.