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According to the Kalika Purana, Kamakhya Temple denotes the spot where Sati used to retire in secret to satisfy her amour with Shiva, and it was also the place where her yoni (genitals, womb) fell after Shiva danced with the corpse of Sati. It mentions Kamakhya as one of four primary shakti peethas: the others being the Vimala Temple within the Jagannath Temple complex in Puri, Odisha; Tara Tarini) Sthana Khanda (Breasts), near Brahmapur, Odisha, and Dakhina Kalika in Kalighat, Kolkata, in the state of West Bengal, originated from the limbs of the Corpse of Mata Sati. This is not corroborated in the Devi Bhagavata, which lists 108 places associated with Sati's body, though Kamakhya finds a mention in a supplementary list.

The Yogini Tantra, a latter work, ignores the origin of Kamakhya given in Kalika Purana and associates Kamakhya with the goddess Kali and emphasizes the creative symbolism of the yoni.

Due to a legendary curse by the Goddess, members of the Koch Bihar royal family do not visit the temple and avert their gaze when passing by.

Historians also have suggested that the Kamakhya temple is an ancient sacrificial site for an Austroasiatic tribal goddess, Kameikha (literally: old-cousin-mother), of the Khasi and Garo peoples; supported by the folk lores of these very peoples. The traditional accounts from Kalika Purana (10th century) and the Yogini Tantra too record that the goddess Kamakhya is of Kirata origin, and that the worship of Kamakhya predates the establishment of Kamarupa (4th century).

The current structural temple and the rock-cut sculpture strewn in the vicinity indicate that the temple has been built and renovated many times in the period 8th–9th, 11th–12th, 13th–14th centuries and even later. The current form, from the 16th century has given rise to a hybrid indigenous style that is sometimes called the Nilachal type: a temple with a hemispherical dome on a cruciform base.The temple consists of four chambers: garbhagriha and three mandapas locally called calanta, pancharatna and natamandira aligned from east to west.

Ancient

The earliest historical dynasty of Kamarupa, the Varmans (350-650), as well as Xuanzang, a 7th-century Chinese traveler ignored the Kamakhya; and it is assumed that the worship at least till that period was Kirata-based beyond the brahminical ambit. The first epigraphic notice of Kamakhya is found in the 9th-century Tezpur plates of Vanamalavarmadeva of the Mlechchha dynasty. Since the archaeological evidence too points to a massive 8th-9th century temple, it can be safely assumed that the earliest temple was constructed during the Mlechchha dynasty. From the moldings of the plinth and the bandana, the original temple was clearly of Nagara type, possibly of the Malava style.

The later Palas of Kamarupa kings, from Indra Pala to Dharma Pala, were followers of the Tantrik tenet and about that period Kamakhya had become an important seat of Tantrikism. The Kalika Purana (10th century) was composed and Kamakhya soon became a renowned center of Tantrik sacrifices, mysticism and sorcery. Mystic Buddhism, known as Vajrayana and popularly called the "Sahajia cult", too rose in prominence in Kamarupa in the tenth century. It is found from Tibetan records that some of the eminent Buddhist professors in Tibet, of the tenth and the eleventh centuries, hailed from Kamarupa.

Medieval

There is a tradition that the temple was destroyed by Kalapahar, a general of Sulaiman Karrani (1566–1572). Since the date of reconstruction (1565) precedes the possible date of destruction, and since Kalapahar is not known to have ventured so far to the east, it is now believed that the temple was destroyed not by Kalapahar but during Hussein Shah's invasion of the Kamata kingdom (1498).

The ruins of the temple was said to have been discovered by Vishwasingha (1515–1540), the founder of the Koch dynasty, who revived worship at the site; but it was during the reign of his son, Nara Narayan (1540–1587), that the temple reconstruction was completed in 1565. According to historical records and epigraphic evidence, the main temple was built under the supervision of Chilarai. The reconstruction used material from the original temples that was lying scattered about, some of which still exists today. After two failed attempts at restoring the stone shikhara Meghamukdam, a Koch artisan, decided to take recourse to brick masonry and created the current dome. Made by craftsmen and architects more familiar with Islamic architecture of Bengal, the dome became bulbous and hemispherical which was ringed by minaret-inspired angashikharas. Meghamukdam's innovation—a hemispherical shikhara over a ratha base—became its own style, called Nilachal-type, and became popular with the Ahoms.

The Koch king issued copper plates endowing land to Brahmans, Daivajana(Astrologers), flower suppliers, garland makers, washermen, cleaners, carpenters, sweet makers, leather workers, cobblers, dancers, singers, weavers, goldsmith, potters, fishermen etc. They were patronised to run the daily routine of the temples.

Banerji (1925) records that the Koch structure was further built over by the rulers of the Ahom kingdom. with remnants of the earlier Koch temple carefully preserved. By the end of 1658, the Ahoms under king Jayadhvaj Singha had conquered the Kamrup and after the Battle of Itakhuli (1681) the Ahoms had uninterrupted control over the temple. The kings, who were supporters of Shaivite or Shakta continued to support the temple by rebuilding and renovating it.

Kamarupa-period stone sculptures in high relief embedded in the walls of the Natamandira constructed by Rajeswar Singha during the Ahom-period.

Rudra Singha (1696–1714) invited Krishnaram Bhattacharyya, a famous mahant of the Shakta sect who lived in Malipota, near Santipur in Nadia district, promising him the care of the Kamakhya temple to him; but it was his successor and son Siba Singha (1714–1744), on becoming the king, who fulfilled the promise. The Mahant and his successors came to be known as Parbatiya Gosains, as they resided on top of the Nilachal hill. Many Kamakhya priests and modern Saktas of Assam are either disciples or descendants of the Parbatiya Gosains, or of the Nati and Na Gosains.