Oconomowoc was incorporated as a town in 1844, although residents had to go to Summit to get their mail until 1845. Travel and communication links between the new town and nearby cities were quickly established. The Watertown Plank Road was extended to connect Oconomowoc to the nearby towns of Milwaukee, Waukesha, Pewaukee, and Watertown in 1850. Such infrastructure encouraged further settlement, and by 1853 the town grew to a population of 250, with ten stores, three hotels, one gristmill, and one sawmill (both located near the present Lake Road bridge), and a schoolhouse. The first passenger train from Milwaukee arrived in Oconomowoc on December 14, 1854, as part of the Milwaukee and Watertown Railroad Company's rapidly expanding Milwaukee & Mississippi line.
In the 1870s, Oconomowoc started to become a summer resort town for wealthy families from the Midwest. Large houses were established around the town's lakes, particularly Oconomowoc Lake and Lac La Belle. The population grew so much that Oconomowoc incorporated as a city in 1865, and by 1880 it had a population of 3,000. In August 1899 a professional golf tournament hosted by the Oconomowoc Country Club was won by Harry Turpie.
In 2003, Oconomowoc acquired Pabst Farms from the Town of Summit. Pabst Farms, which had previously been owned by the Pabst family, is being developed as a mixture of commercial and residential property. On April 2, 2008, a gas line exploded just west of downtown, destroying the First Baptist Church on West Wisconsin Avenue. The church, which was built in 1913, was completely destroyed, except for the frame of its bell tower, which later had to be torn down as it was at risk of collapse. The source of the explosion was an old gas line that had been capped off sometime in 1972–73; it ruptured after having been struck by a backhoe as utility work was being done on Wisconsin Avenue in preparation for reconstruction of the street.