Unofficial returns showed Democrats unseating at least a dozen Republicans and flipping three seats that had been occupied by GOP incumbents who did not seek reelection. Four other races were so close that they qualify for a recount, and the outcome will determine control of the chamber. The results marked the most sweeping shift in control of the legislature since Reconstruction.
Republicans, who have controlled the chamber since 2000, went into Tuesday holding 66 of 100 seats. Democrats fielded the most candidates in recent memory, including a record number of women.
Control of the chamber may not be determined for days as provisional ballots are counted in narrow races.
Democrats need to hold one seat where they are narrowly leading to ensure a 50-50 split where power sharing would be necessary, and to pick up an additional seat in a race eligible for a recount to take full control of the chamber.
The election signaled a major shift in the gender of a body long dominated by men: Of the 15 seats Democrats flipped, all were held by men and 11 were won by women. Several of those women made history.
One became Virginia's first openly transgender person to win elective office, unseating an opponent of LGBT rights. Another became the first open lesbian elected to the House of Delegates, another the first Asian American woman and two, both from diverse Prince William County, are set to be the first Latinas elected to the General Assembly.
"This is an unbelievable night," said House Minority Leader David J. Toscano (D-Charlottesville) in an interview an hour after polls closed. "There were districts we didn't think we had much of a shot in."
Democrats benefited from gubernatorial contender Ralph Northam's coattails: He won by nine percentage points.
"Obviously, tonight was a difficult night, and the outcome is not what anyone expected," said Matt Moran, spokesman for the House Republican Caucus. "We also want to thank our colleagues and fellow Republican candidates who ran principled campaigns based on positive ideas in a difficult political environment. Our team is closely monitoring the canvasses that will take place tomorrow as we await the official results."
Although House races are normally seen as the sleepy backwater to the gubernatorial contest, they generated a surge of interest this year from activists energized by President Trump's election and new groups that see the legislative contests as an opportunity to test strategies and technologies ahead of next year's elections.
Strategists said the results suggest trouble for Republicans.
"This is a tidal wave," said David Wasserman, an analyst who tracks U.S. House races for the nonpartisan Cook Political Report. "It's hard to look at tonight's results and to conclude anything other than that Democrats are the current favorite for control of the House in 2018."
The highest-spending House of Delegates race was in southwest Virginia, where former television news anchor Chris Hurst, whose girlfriend was fatally shot during a live broadcast in 2015, challenged Republican incumbent Joseph Yost.
Both raised more than $1 million for their bids, and Hurst won.
A pair of Democratic incumbents easily fended off well-financed challenges by Republicans. Subba Kolla, who would have been the body's first Indian American lawmaker, lost to Del. John J. Bell in Loudoun County, and Heather Cordasco fell to Del. Michael P. Mullin in Hampton Roads.
Democrats flipped the most seats in Northern Virginia as Northam posted a strong showing in the populous region. If results hold, Democrats will hold every delegate seat in Arlington, Alexandria, Fairfax and Prince William counties — and all but one in Loudoun County.
The biggest battleground for the House was Prince William, a Washington exurb where people of color constitute a majority of the population. A diverse group of five Democratic challengers hoped to channel demographic changes and Democratic energy to take seats held by white men — and all won.
Danica Roem, who will be Virginia's first openly transgender elected official, defeated Del. Robert G. Marshall (R-Prince William), a culture warrior who opposes LGBT rights. Elizabeth Guzman, who raised more money than any Democratic candidate except for Hurst, unseated Del. L. Scott Lingamfelter (R-Woodbridge).
Republican Dels. Richard L. Anderson (Prince William) and Jackson H. Miller (Manassas) lost to their Democratic challengers, Hala Ayala and Lee Carter. Ayala and Guzman are Latina, and Carter is a member of the Democratic Socialists of America.
In an open seat vacated by a retiring Republican, Democrat Jennifer Carroll Foy easily defeated Republican Michael Makee.
In Fairfax County, Democrat Kathy Tran, the daughter of Vietnamese refugees, beat Republican Lolita Mancheno-Smoak for an open seat vacated by retiring Del. David B. Albo (R), while Democrat Karrie Delaney handily defeated Del. James M. LeMunyon (R). Del. Timothy D. Hugo, the Republican caucus chairman, was narrowly trailing Democratic challenger Donte Tanner, and the results were within the margin for a state-funded recount. Hugo picked up 100 votes during a Fairfax County canvass on Wednesday morning.
With nearly all precincts reporting in Loudoun County, Del. Thomas A. "Tag" Greason (R) was set to lose to Democratic challenger David Reid in that county's most competitive race in a district that Hillary Clinton carried by 19 points a year ago.
Greason's fellow Loudoun County lawmaker, Del. J. Randall Minchew, lost his seat to Democratic challenger Wendy Gooditis. Another Loudoun County Republican lawmaker, David A. LaRock, defeated his Democratic challenger, Tia Walbridge — and may be the lone Republican left representing Northern Virginia in the House.
In the Richmond suburbs, Dels. John M. O'Bannon III and G. Manoli Loupassi lost their seats to Debra Rodman and Dawn Adams, who is openly lesbian. Democrat Schuyler T. VanValkenburg won an open seat vacated by Republican Jimmie Massie III.
In the Virginia Beach area, Del. Ronald A. Villanueva lost to Democrat Kelly Fowler, while N.D. "Rocky" Holcomb III lost to Cheryl Turpin in a squeaker. Del. Glenn R. Davis Jr. narrowly pulled out a win for reelection.
Republicans were barely leading in three contests that were in the margin for a recount, including in the race to succeed retiring Speaker William J. Howell (R-Stafford). Del. David Yancey (R-Newport News) led Shelly Simonds by only 12 votes.
Even if Democrats fall short of taking control of the chamber this year, they see a potential for additional pickups next year, if a court challenge of legislative district maps forces special elections, and in 2019 when all 100 seats are on the ballot again.
Republicans have a narrow 21-to-19 majority in the state Senate, where all seats are up in 2019.
Control of the governor's mansion and legislature in Virginia has national implications. The General Assembly will draw congressional and state legislative district maps after the 2020 Census, and the governor has the power to veto those maps.
Maria Sacchetti and Jenna Portnoy contributed to this report.