The settlement was originally named Bentley Manor by one of its first settlers, Captain Christopher Billop (1638–1726), a member of the Royal Navy, after his own ship.

In 1869 it was renamed as Tottenville after John Totten and his prominent local family of that name, some of whom served as Loyalists under Billop during the American Revolutionary War.

[4] The Raritan band of the Unami Indians, a branch of the Lenape or Delaware nation, were the original inhabitants of all Staten Island, including Tottenville.

[5] During the colonial period and for a significant time thereafter, Tottenville was an important waypoint for travelers between New York City—of which Staten Island did not formally become a part until 1898—and Philadelphia.

Two distinctive landmarks stand at the northern approaches to the neighborhood: the Bethel United Methodist Church, erected in 1840 and rebuilt on the same site in 1886 after a fire destroyed the original structure.

The Conference House was built by Christopher Billop and so named because it was the site of negotiations to end the American Revolutionary War in 1776, but these were unsuccessful.

[6] Tottenville has a strong Victorian architecture heritage, akin to neighborhoods on Staten Island's North Shore.

During an early period of industrialization, many small factories once dotted the neighborhood's western shoreline, but jobs have shifted and most are no longer in operation.

After the decrease in waterfront industries and decades of working to improve water quality, in 2005, the city approved oyster harvesting again.

During the 1990s, the section of Tottenville southeast of Hylan Boulevard, until then nearly uninhabited, was an area of intense levels of new home construction.

A second commercial core began to emerge at the north end of the community along Page Avenue and west of Amboy Road at this time.

The fate of 7484 Amboy Road, built circa 1870 as the parsonage of Bethel Methodist Church and contained an extremely large backyard, became the focus of an intense local controversy in March 2005.

The community opposed plans by builder John Grossi, who had purchased the property, to raze the house and construct five townhouse units on the site.

The public outcry prompted New York City mayor Michael Bloomberg to have the home declared a landmark, and prevented its demolition.

Bloomberg announced his decision during a visit to Tottenville on March 22, and the New York City Landmarks Preservation Commission made the designation official on April 12.

In 2016, a consortium of Bridgewater Capital and the Brooklyn-based Riseman family bought 30 acres (12 ha) of the Nassau Smelting property from Lucent Technologies.

For census purposes, the New York City government classifies Tottenville as part of a larger neighborhood tabulation area called Charleston-Richmond Valley-Tottenville.

[2] In 2018, an estimated 11% of Tottenville and the South Shore residents lived in poverty, compared to 17% in all of Staten Island and 20% in all of New York City.

Based on this calculation, as of 2018[update], Tottenville and the South Shore are considered high-income relative to the rest of the city and not gentrifying.

In January 1969 it re-opened as the New Stadium Theatre and was a rock-music venue hosting bands such as The Brooklyn Bridge.

[22] Tottenville is served by the New York City Fire Department (FDNY)'s Engine Co. 151/Ladder Co. 76, located at 7219 Amboy Road.

In 2018, this population of uninsured residents was estimated to be 4%, less than the citywide rate of 12%, though this was based on a small sample size.

[10]: 14 The concentration of fine particulate matter, the deadliest type of air pollutant, in Tottenville and the South Shore is 0.0066 milligrams per cubic metre (6.6×10−9 oz/cu ft), less than the city average.

[26] The United States Postal Service operates one post office in Tottenville, located at 228 Main Street.

[27] Tottenville and the South Shore generally have a similar rate of college-educated residents to the rest of the city as of 2018[update].

[10]: 6  The percentage of Tottenville and the South Shore students excelling in math rose from 48% in 2000 to 65% in 2011, though reading achievement declined from 55% to 52% during the same time period.

[28] Tottenville and the South Shore's rate of elementary school student absenteeism is lower than the rest of New York City.

[11]: 24 (PDF p. 55) [10]: 6  Additionally, 89% of high school students in Tottenville and the South Shore graduate on time, more than the citywide average of 75%.