The church's original name was precise and somewhat architectural: Saint John the Forerunner by-the-Dome, in Greek Hagios Ioannis ho Prodromos en tō Trullō. The 'Trullos' in the name referred to a dome-roofed palace that stood somewhere in the neighborhood — 'troullos' in Greek means dome, cognate with the Italian 'trullo.' Constantinople had at least 36 churches dedicated to Saint John the Baptist, which gives some sense of how dense the city's religious fabric was. This particular one was part of a monastery, later housing a small community of nuns. The style of its construction dates the building to the twelfth century, though nothing is known of its history before the Ottoman conquest of 1453.

After Constantinople fell in 1453, the new Ottoman administration permitted the continuation of Christian worship under the Ecumenical Patriarchate, but the institutional landscape shifted constantly in those early years. When Patriarch Gennadios moved the Patriarchate from the Church of the Holy Apostles to the nearby Pammakaristos church between 1454 and 1456, nuns who had been living at Pammakaristos were relocated to the small nunnery of Troullos — probably established on this occasion. For over a century the nuns maintained their community in what had been, and remained, a functioning Byzantine church within an Ottoman city. That arrangement ended toward the close of the sixteenth century.

Hırami Ahmet Pasha served as Agha of the Janissaries — commander of the elite Ottoman infantry — before rising to the rank of Pasha under Sultan Murat III. In the late 1580s he was responsible for converting the Pammakaristos church itself into a mosque, a landmark act that removed one of the last remaining major Christian institutions from the old city center. He then turned to the small church of Saint John as well, closing the nunnery and expelling the nuns who had lived there, and converting the building to Islamic use. The conversion likely took place between 1587 or 1588, when the Pammakaristos conversion occurred, and 1598, the year of his death. The diaconicon — a service room in Byzantine church architecture — was repurposed as the mosque's mihrab, the niche indicating the direction of Mecca.

By the early twentieth century the small building had fallen into serious disrepair. The narthex was nearly destroyed, the columns had vanished, and whatever paintings remained on the interior walls were barely legible. A careful restoration in 1961 stabilized the structure and returned it to active use as a mosque. Four replacement columns were installed in place of the missing originals; their exact origin is not known. The three semicircular apses survive, including the projecting central apse with its large window divided into three sections. Barrel vaults cover the north and south arms of the cross-shaped plan, and four columns with capitals carry an octagonal drum supporting the dome. The building has never been the subject of a systematic archaeological or architectural study — remarkable for a structure of its age and uniqueness.

The Hirami Ahmet Pasha Mosque sits in Koltutçu Sokak in the Çarşamba neighborhood, one of the most religiously conservative areas of the old walled city — a setting that makes its continued function as a mosque feel continuous with the neighborhood around it, even as the building itself predates the Ottoman period by several centuries. Less than 400 meters to the north stands the Pammakaristos, now the Fethiye Mosque and Museum. Between them, in the dense streets of Fatih, a thousand years of Byzantine and Ottoman history press close. The church that became a mosque without a minaret is easy to miss. That may be part of why it survived.