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Fukushima has the third highest population in the prefecture, behind the cities of Iwaki, with 377,288, and Kōriyama, with 336,328. This makes Fukushima the only prefectural capital in Japan that is the third largest city in the prefecture. The Fukushima metropolitan area had a May 2011 estimated population of 452,912 and consisted of the towns and cities of Nihonmatsu, Date, Kunimi, Koori, Kawamata, and Fukushima. It is the second most populous metropolitan area in Fukushima Prefecture, with the Kōriyama metropolitan area being the largest with a population of 553,996. The Fukushima metropolitan area is also the sixth largest metropolitan area in the Tōhoku region.

In ancient Japan, the area now known as Fukushima City was called Minekoshi (岑越). The mountain in the middle of the city, present day Mt. Shinobu, was also formerly called Mt. Minekoshi (岑越山). During the Jōmon period, for around 2,000 years there was a large settlement on the eastern bank of the Abukuma River. This area has since been excavated and named the Miyahata Site. In the 5th century AD, Kumano Atai (久麻直) was appointed by the Yamato period (Yamato court) to be the Kuni no miyatsuko (信夫国造), giving him control over the Fukushima Basin. Under the Nara period's Ritsuryō system, stations were established along the Seven Circuits so that officials could change horses. One of the stations, the Tōsandō, passed through the area of present day Fukushima, and Minekoshi Station was established on the route. Minekoshi Station was located south of the Surikami River and north of the Matsukawa River, which at the time flowed to the south of Mt. Minekoshi. The area south of the Matsukawa River was then, as it still is now, known as Suginome (杉妻). Thus it is believed that the station was located north of the area around the present day prefectural office, in the Kita gorōuchi area (北五老内地域). The implementation of the Ritsuryō system also resulted in administrative changes, with the area of present day Fukushima and Date being combined to form the district of Shinobu. This was the northernmost point of the Mutsu Province and held responsibility for preventing the southern expansion of the Emishi, a people who lived in northern Honshū. After 718, and the widening influence of the Yamato Imperial Court, Mutsu Province was expanded northwards into present day Miyagi Prefecture. Along with this redrawing of boundaries, present day Fukushima Prefecture was separated from the new Mutsu Province (approximately present day Miyagi) and split between the newly formed provinces of Iwaki in the east and Iwase in the west. However, by 724 Mutsu Province was unable to deal on its own with the economic costs of holding back the Emishi, so Iwaki and Iwase provinces were merged back into Mutsu. In the first half of the 10th century, the Date district was separated from the Shinobu district. As a reform to the sōyōchō (租庸調) tax on rice, labor, and textiles, there was a nationwide effort from the Imperial Court to split up districts so they each had approximately the same population. This was accomplished both through administrative changes and forced population relocations. With Mutsu Province viewed as reclaimed land by the Imperial Court, the area saw a significant amount of reorganization. In the late Heian period, almost the entirety of the Tōhoku region was ruled by the Northern Fujiwara clan. Relatives of the Northern Fujiwara clan, the Shinobu Satō clan (信夫佐藤氏) was given domain over nearly the entirety of present day Fukushima Prefecture's centrally located Nakadōri area and eventually expanded their control to include Aizu to the west as well. It is said that the Shinobu Satō clan is one of the reasons for the Satō surname spreading throughout and eventually becoming the most common surname in Japan.

In 1180, Minamoto no Yoshitsune, was accompanied by Shinobu district residents Satō Tsugunobu (佐藤継信) and Satō Tadanobu (佐藤忠信) on his way south to Kantō to fight the Taira clan in the Genpei War. In 1413, Date Mochimune (伊達持宗) shut himself inside Daibutsu Castle (大仏城) in defiance of the Kamakura kubō. This is the first known historical mention of Daibutsu Castle, which was near the confluence of the Abukuma and Arakawa rivers at the present day location of the Fukushima Prefectural Offices. It is said that the castle was named after the "Suginome Great Buddha" (杉妻大仏), a Vairocana Buddha statue kept within the castle. The castle was also known as Suginome Castle (杉妻城). It is believed that in this time period the area's name was changed from Minekoshi to Suginome (杉妻) to reflect the concentration of political power in the area. During the Azuchi–Momoyama period, in 1591 Gamō Ujisato gained control of the Shinobu and Date districts, and under him Kimura Yoshikiyo (木村吉清) took control of Ōmori Castle (大森城), which was in the southwest of present day Fukushima. The following year he moved from Ōmori Castle to Suginome Castle. It is said that, inspired by the recent renaming of "Black River Castle"; 黒川城; Kurogawa jō to the more joyous sounding "Young Pine Castle"; 若松城; [[Wakamatsu Castle, he changed the name of his new residence to "Lucky Island Castle"; 福島城; Fukushima jō. Train services were also stopped due to damage caused to railway infrastructure. The Iizaka Line reopened two days later on March 13, and on March 31 the Yamagata Shinkansen resumed limited service and the Ōu Main Line resumed full service. By April 7 the Tōhoku Main Line was reopened in both directions, however it was closed again following a strong earthquake later that night. The Tōhoku Main Line was again reopened in both directions from Fukushima on April 17. The Tōhoku Shinkansen reopened with limited service on April 23, and the Abukuma Express Line resumed limited service from Fukushima on April 28. On April 1, 2018, Fukushima City became a core city.

Fukushima has a mayor council form of government with a directly elected mayor and a unicameral city legislature of 35 members. The city also contributes eight members to the Fukushima Prefectural Assembly. In terms of national politics, most of the city falls within the Fukushima 1st district, a single member constituency of the House of Representatives in the national Diet of Japan, which also includes the cities of Date, Sōma, Minamisōma and Date District and Sōma District.

As of 2005, the total income of all citizens of Fukushima totalled trillion. Of this income, 0.8% was made in the primary sector, 24.1% in the secondary sector, and 80.1% in the tertiary sector. Income in the primary sector was led by that from agriculture, which totaled The secondary sector was led by general manufacturing, with income there totaling billion. The service industry led the tertiary sector with a total income of billion. Fruits by far make up the largest value of crops grown in Fukushima, led by an annual production of 14,935 tons of apples, 13,200 tons of Japanese pears, and 11,517 tons of peaches. While Fukushima produces more apples and pears than peaches, as a percentage of national fruit production, in 2010 Fukushima produced 8.2% of all peaches grown in the country, compared to 5.1% of all Japanese pears and 2.3% of all apples. When the neighboring cities of Date, Kunimi and Koori, all of which are also in the Fukushima Basin, are taken into effect, the Fukushima metro area produced 20.1% of all peaches grown in Japan in 2010. The city is known for its many peach, pear, apple, and cherry orchards which are located throughout the city, especially along the so called Fruit Line (フルーツライン) road that loops the western edge of the city. Fukushima is also sometimes known as the Fruit Kingdom (くだもの王国).

In 2009 Fukushima's industries directly employed 18,678 workers and shipped ¥671 billion worth of goods. This was led by information related industries with 50.5% of total output. Other industries in Fukushima include those dealing with food at 7.6% of total output, metals at 7.5%, chemistry at 5.3%, ceramics at 4.9%, electricity at 4.5%, printed goods at 2.8%, steel at 2.5%, plastics at 2.5%, and electronics at 2.2%. Other various industries make up the final 9.8%. In 2009, the value of goods shipped by Fukushima's industries comprised 14.2% of all of Fukushima Prefecture's total output for the year.

Due to Fukushima having long been the junction of the Ōshū Kaidō and Ushū Kaidō routes, it has developed into an important transportation hub. It is currently the location of where National Route 13 breaks off from National Route 4. Fukushima Station is where the Ōu Main Line separates from the Tōhoku Main Line and the Tōhoku Shinkansen separates from the Yamagata Shinkansen.

For automobile traffic, Fukushima is linked to Tokyo in the south and Aomori in the north via the Tōhoku Expressway, which passes through Fukushima and has multiple interchanges within the city. There are six national highways that run from or through Fukushima. Japan National Route 4 runs to Tokyo in the south, through Fukushima, then north to Sendai and beyond; Japan National Route 13 begins in Fukushima, runs through Yamagata Prefecture, then terminates in Akita Prefecture; Japan National Route 114 starts in Fukushima and runs southeast to the town of Namie; Japan National Route 115 runs through Fukushima, connecting Sōma in the east to Inwashiro in the west; Japan National Route 399 starts southeast of Fukushima in the city of Iwaki, Fukushima, continues northwest through Fukushima, and terminates in the city of Nan'yō, Yamagata; and Japan National Route 459 begins in Niigata, Niigata, runs eastward through Kitakata, through Fukushima, southward to Nihonmatsu, then eastward to Namie. Also within the city is the Bandai Azuma Skyline scenic toll road, which runs up and along Mt. Azuma on the western edge of the city, connecting Takayu Onsen and Tsuchiyu Onsen. Local bus services throughout the city and region are primarily operated by Fukushima Transportation. Local bus service to the Kawamata area is offered by both JR Bus Tōhoku and Kanehachi Taxi. Intercity buses are operated by a multitude of companies and link Fukushima to the cities of Iwaki, Aizuwakamatsu, and Kōriyama within the prefectures and to the Sendai, Tokyo, and Kinki areas outside the prefecture, among others.

There is no commercial airport within the city limits. For air transportation, Fukushima is served by both Fukushima Airport in the city of Sukagawa and Sendai Airport in Natori, Miyagi.

The city is home to the Fukushima Azuma Baseball Stadium, which was an Olympic venue at the Tokyo 2020 Summer Olympics. Fukushima United football club play at the athletic Toho Stadium. The city's third professional team is basketball Japanese Second Division club Fukushima Firebonds.