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The first urban settlement in the area of Celje appeared during the Hallstatt era. The settlement was known in the Celtic times as Kelea; Celts coined money in the region.

Once the area was incorporated in the Roman Empire, it was known as Civitas Celeia. It received municipal rights in AD 46 under the name municipium Claudia Celeia during the reign of the Roman Emperor Claudius (41-54). Written records suggest that the town was rich and densely populated, secured with the walls and towers, full of multi-storied marble palaces, wide squares, and streets.

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It was called Troia secunda, or the second or small Troy. A Roman road through Celeia led from Aquileia (Sln. Oglej) to Pannonia. Celeia soon became one of the most flourishing Roman colonies, and possessed numerous great buildings, of which the temple of Mars was famous throughout the whole empire. Celeia was incorporated with Aquileia ca. 320 under the Roman Emperor Constantine I (272-337).

The city was razed by Slavic tribes during the Migration period of the 5th and 6th century, but was rebuilt in the Early Middle Ages. The first mention of Celje in the Middle Ages was under the name of Cylie in Admont's Chronicle, which was written between 1122 and 1137.

The town was the seat of the Counts of Celje from 1341 to 1456 It acquired market-town status in the first half of the 14th century and town privileges from Count Frederick II on April 11, 1451.

Gosposka Street with the Cathedral of the Prophet Daniel in the backgroundAfter the Counts of Celje died out in 1456, the region was inherited by the Habsburgs of Austria and administered by the Duchy of Styria. The city walls and defensive moat were built in 1473. Many local nobles converted to Protestantism during the Protestant Reformation, but the region was converted back to Roman Catholicism during the Counter-Reformation. Celje became part of the Habsburgs' Austrian Empire during the Napoleonic Wars. In 1867, after the defeat of Austria in the Austro-Prussian War, the town became part of Austria-Hungary.

The first train of the Vienna-Trieste railway line came to Celje on April 27, 1846. In 1895 the Celje secondary school, established in 1808, taught Slovene.

At the end of the 19th century and in the early 1900s, Celje was a strong center of German nationalism against Slovenes. The 1910 census showed an 66.8% German population. A symbol of this was the German Cultural Center(German: Deutsches Haus), built in 1906 and opened on May 15, 1907, today the Celje Hall (Slovene: Celjski dom). Even the centuries-old German name of the town, Cilli, sounded no longer German enough to German ears so that the form Celle was preferred by many. The 1911 Encyclopædia Britannica listed the town, which in 1900 had 6,743 and in 1924 had 7,750 citizens, under the German name Cilli. The National Hall (Narodni dom), which hosts the seat of a township today, was built in 1896. The first telephone in the city was installed in 1902 and the city received electric power in 1913.

Celje, Georg Matthäus Vischer, Topographia Ducatus Stiriae, Graz 1681Slovene and German ethnic nationalism increased during the 19th and early 20th centuries. With the collapse of Austria-Hungary in 1918 as a result of World War I, Celje became part of the Kingdom of Serbs, Croats and Slovenes (later known as Yugoslavia). During this period, the town experienced a rapid industrialization and a substantial growth in population.

Celje was occupied by Germany in April 1941. The Gestapo came to Celje on April 16, 1941 and were followed three days later by SS leader Heinrich Himmler, who inspected Stari pisker. During the war the city also suffered from allied bombing of important communication lines and military installations. The National Hall was severely damaged.

The toll of the war on the city was terrible. The city (including nearby towns) had a pre-war population of 20,000 and lost 575 people during the war, mostly between the ages of 20 and 30. More than 1,500 people were deported to Serbia or into the interior of the German Third Reich. Around 300 people were interned and around 1,000 people imprisoned in Celje's prisons. An unknown number of citizens were forcibly mobilized in the German army. Around 600 "stolen children" were taken to Nazi Germany for germanization. A monument in Celje called Vojna in mir (War and Peace) by the sculptor Jakob Savinšek, commemorates the World War II era.

Celje southwards on the picture from 1750. The Voglajna River on the left flows into the Savinja River (German: Sann), which then flows to its end in the Sava River. On the right of the Savinja an island can be seen; today the district that covers the island is called Otok, which is Slovene for 'island'.
War and Peace monument (Vojna in mir) by Jakob SavinšekAfter the end of the war, the remaining German-speaking portion of the populace was expelled. The new communist government took advantage of existing anti-tank trenches, dug around Celje by the retreating German army, by using them as mass graves. They were filled with Croatian, Serbian, and Slovenian militia members who had collaborated with the Germans, as well as civilians who had opposed either the national liberation movement or the communist revolution during the war, civilians of German descent or simply individuals accused or suspected of anti-communism. The purpose was to physically eliminate any potential political opposition. On the pretext of collaboration with the enemy, the Yugoslav National Army executed more than 30,000 - mostly Croat, German and Slovenian - prisoners in the Celje area, without any judicial process. The bodies were buried in hidden mass graves in Celje; the exact number is still not known. At the concentration camp at Teharje, some 5,000 Slovenians, hundreds of them still minors, were murdered within two months after the end of the war, again without trial. Furthermore, refugee trains carrying German civilians from the "Rann triangle" area were halted near Celje on August 5, 1945 and their passengers sent to a concentration camp at Teharje. After the camp was abolished in 1950, the local authorities established a huge industrial dump over the graveyard there, concealing the evidence of killings under a mound of toxic waste. In 1991, when it became possible again to discuss the facts pertaining to the massacre, the Slovenian government decided to build a memorial to the victims of Teharje.

Celje became part of independent Slovenia after the Ten-Day War in 1991. On April 7, 2006, Celje became the seat of a new Diocese of Celje, created by Pope Benedict XVI within the Archdiocese of Maribor. The town's tourist sights include a Minorite monastery founded in 1241 and a palace from the 16th century.