Okulovka was first mentioned in the cadastres of the Derevskaya Pyatina of the Novgorod Land in 1495. In 1851, Okulovka became a station of the Nikolayevskaya Railway.
In the mid-19th century, on his land in Parakhino, 4.3 km from the Okulovka station, industrialist Vladimir Pasburg founded a stationery factory that produced wrapping paper from rags and worn-out bast shoes. A little later, at the confluence of the Khorenka and Peretna rivers, professor of medicine N. Bardashevich founded the Kulotinskaya Factory that produced sack canvas.
The station town of Okulovka started to grow fast. A small brick factory was built in next to no time. Eight landowners, five contractors, twenty merchants, five priests and 15 police officers built estates and houses in the small town. There was a merchants’ club, a four-year railway school, a parish school and a private school.
Two St Nicholas churches and a wooden Church of the Holy Mother of God, transferred from Mshentsy, were built, along with an almshouse and a peasant house. There was also a rural hospital with one doctor.
On 12 January 1965, the Presidium of the RSFSR Supreme Council issued an order to grant Okulovka the status of a town, merging two towns, Parakhino-Poddubye and Okulovka-1, into one administrative entity.