The city sits on the ruins of the original Kirkuk Citadel, site of the ancient mid 3rd millennium BC, Assyrian city of Arrapha, and which sits near the Khasa River. The city is mentioned during the Sumero-Akkadian period of Assyria in cuneiform script from about 2400 BC. The region became a part of the Akkadian empire (2335–2154 BC) which united all of the Akkadian and Sumerian speaking Mesopotamians under one rule. After its collapse, the language isolate speaking Gutians, a pre-Iranic race from Ancient Iran, overran the region for a few decades, making Arrapha their capital, before being ejected from Mesopotamia by the Sumerians during the Neo-Sumerian Empire (2112–2004 BC). The city later came to be dominated by the Hurrians from eastern Anatolia before being incorporated into the Old Assyrian Empire (2025–1750 BC), after which Arrapha and the whole of northern Mesopotamia, together with parts of north east Syria and south east Turkey, became a part of Assyria proper. During the late 15th century BC Assyria and Arrapha was under the domination of the short-lived Mittani-Hurrian empire, but after the Assyrians overthrew and destroyed the Hurri-Mitanni in the early 14th century BC the city was once more under Assyrian rule. Arrapha remained an important Assyrian city until the fall of the Assyrian empire between 615–599 BC. After this it remained a part of the geo-political province of Assyria (Achaemenid Assyria, Athura, Seleucid Syria, Assyria (Roman province) and Assuristan) under various foreign empires, and between the 2nd century BC and 3rd century AD became the capital of the Neo-Assyrian state of Beth Garmai before this was conquered into the Sassanid empire and became a part of Assuristan. The Arab Islamic conquest of the 7th century AD saw the dissolution of Assyria as a geo-political entity.
Kurds and Turkmens have claimed the city as a cultural capital. It was named the "capital of Iraqi culture" by the Iraqi ministry of culture in 2010. The city currently consists mainly of people who self-identify as Kurds, Arabs, Iraqi Turkmens and Assyrians, with changes in population after the fall of Saddam Hussein, the US invasion, and the war against the Islamic State.
The ancient name of Kirkuk was the Assyrian Arrap'ha. During the Parthian era, a Korkura/Corcura (Ancient Greek: Κόρκυρα) is mentioned by Ptolemy, which is believed to refer either to Kirkuk or to the site of Baba Gurgur 4.5 kilometres (2.8 mi) from the city. Since the Seleucid Empire it was known as Karkha D-Bet Slokh, which means 'Citadel of the House of Seleucid' in Mesopotamian Aramaic, the lingua franca of the Fertile Crescent in that era.
The region around Kirkuk was known historically in the Eastern Aramaic and Syriac Assyrian sources as "Beth Garmai" (Syriac: ܒܝܬܓܪܡܝ). The name "Beth Garmai" or "Beth Garme" may be of Syriac origin which meaning "the house of bones", which is thought to be a reference to bones of slaughtered Achaemenids after a decisive battle between Alexander the Great and Darius III on the plains between the Upper Zab and Diyala river. It was one of a number of independent Neo-Assyrian states which flourished during the Parthian empire (150 BC-226 AD). Kirkuk itself was the Assyrian Karkha D'Beth Slokh, the metropolitan centre of Beth Garmai.