Zhuhui District derives its name from the historic Zhuhui Pagoda within its territory.

In the Spring and Autumn Period, the area belonged to the Chu State. During the Qin Dynasty, it was administered under Changsha Commandery. In 202 BCE (the 5th year of Emperor Gaozu of Han), Ling County was established with its seat at present-day Hudong Village, Heping Township, Zhuhui District, remaining under Changsha Commandery. 

In 196 CE (the 1st year of Jian'an era, Eastern Han Dynasty), Linzheng County was established through the territorial reorganization of the northeastern sector of Ling County's southern district and the eastern sector of Zhengyang County, with its administrative seat maintained at the former Ling County capital. 

In 220 CE (Three Kingdoms period), Xiangdong Commandery was established from southeastern Changsha Commandery, with its capital at Ling County. During the Sui, Tang and Song dynasties, the territory remained part of Hengyang County. 

In 1337 (the 3rd year of Zhiyuan era, Yuan Dynasty), it was governed under Xincheng County of Hengzhou Route, Huguang Province. In 1377 (the tenth year of Hongwu era, Ming Dynasty), it belonged to Hengyang County under Hengzhou Prefecture. 

In 1756 (the 21st year of Qianlong era, Qing Dynasty), Zhuhui was incorporated into Qingquan County under Hengzhou Prefecture, Heng-Yong-Chen Route, Hunan Province. 

In 1913 (the 2nd year of Republic of China), it became part of Hengyang County. In 1914 (the 3rd year of Republic of China), jurisdiction transferred to Hengyang Route. In 1920 (the 9th year of Republic of China), all counties came under direct provincial administration. 

On January 1, 1942, the area was designated as the fifth district under municipal administration. In August 1949, it returned to Hengyang County. On October 8, 1949, it became the fifth district again before being reclassified as the third district in September 1951. In May 1955, it was officially named Jiangdong District. 

On April 23, 1960, the district was restructured as "Jiangdong District People's Commune of Hengyang". In 1961, Shiziling and Hubei Road sub-communes were abolished while Dongyangdu sub-commune was established. 

In June 1977, Xinxiang Subdistrict was created. In January 1982, Hunan Road Subdistrict was renamed Guangdong Road Subdistrict. 

In April 2001, Hengyang's urban redistricting renamed Jiangdong District as Zhuhui District, incorporating Chashan'ao Town, Dongyangdu Town, Heping Township and Linghu Township from the former suburban area. 

On November 17, 2006, Wangjiang Village and Maoping Village from Xiantang Town, Hengnan County were transferred to Linghu Township. On September 5, 2007, these villages were separated to establish Hengzhou Road Subdistrict.