St. John's County Homes With Guest Suite

Are you a home buyer who could use the extra living space a guest suite provides? Featured here are all St. John's County homes for sale with a guest suite. If you’re interested in any of the St. John's County guest suite home listings that you see below, just click the "Ask a Question" button when viewing the details of that property. Our St. John's County real estate agents can provide you with disclosures, past sales history, dates and prices of properties recently sold nearby, and other details related to St. John's County homes with a guest suite.

And if you'd like to stay up-to-date on St. John's County homes with a guest suite, we also invite you to register for a free account so that you can receive email alerts whenever new listings hit the market that fit your search criteria, allowing you to stay one-step ahead of other buyers in the area. And remember to call or text us directly with any additional questions you have about buying or selling a home in St. John's County, Florida. 

Search St. John's County Homes With Guest Suite

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New
317 Ponte Vedra Boulevard, Ponte Vedra Beach

$12,000,000

317 Ponte Vedra Boulevard, Ponte Vedra Beach

7 Beds 7 Baths 4,600 SqFt Residential MLS® # 2047619
New
1120 N St. Johns Street, St Augustine

$305,000

1120 N St. Johns Street, St Augustine

3 Beds 2 Baths 1,226 SqFt Residential MLS® # 2047616
New Pending
142 Latham Drive, Ponte Vedra

$536,230

142 Latham Drive, Ponte Vedra

2 Beds 2 Baths 1,784 SqFt Residential MLS® # 2047611
New
75 Yorkshire Drive, St Augustine

$872,990

75 Yorkshire Drive, St Augustine

5 Beds 4 Baths 2,903 SqFt Residential MLS® # 2046712
New
91 Ridgewind Drive, St Augustine

$569,900

91 Ridgewind Drive, St Augustine

4 Beds 3 Baths 2,357 SqFt Residential MLS® # 2047511
New
323 Seagrove Drive, Ponte Vedra

$1,599,000

323 Seagrove Drive, Ponte Vedra

5 Beds 5 Baths 4,068 SqFt Residential MLS® # 2046397
New
105 Prince Albert Avenue, St Johns

$499,900

105 Prince Albert Avenue, St Johns

4 Beds 3 Baths 2,492 SqFt Residential MLS® # 2047589
New
1001 W Aiken Street, St Augustine

$349,990

1001 W Aiken Street, St Augustine

3 Beds 3 Baths 1,465 SqFt Residential MLS® # 2047567
New
994 W Aiken Street, St Augustine

$349,990

994 W Aiken Street, St Augustine

3 Beds 3 Baths 1,465 SqFt Residential MLS® # 2047566
New
901 Scheidel Way, St Augustine

$349,990

901 Scheidel Way, St Augustine

3 Beds 3 Baths 0 SqFt Residential MLS® # 2047565
New
895 Scheidel Way, St Augustine

$349,990

895 Scheidel Way, St Augustine

3 Beds 3 Baths 0 SqFt Residential MLS® # 2047564
New
845 Avery Street, St Augustine

$349,990

845 Avery Street, St Augustine

3 Beds 3 Baths 1,465 SqFt Residential MLS® # 2047563
New
171 Beale Avenue, St Augustine

$430,000

171 Beale Avenue, St Augustine

3 Beds 2 Baths 1,643 SqFt Residential MLS® # 2047557
New
103 Reflections Avenue, Ponte Vedra

$859,990

103 Reflections Avenue, Ponte Vedra

4 Beds 3 Baths 2,464 SqFt Residential MLS® # 2047545
New
312 Whirlwind Place 182, St Augustine

$494,990

312 Whirlwind Place 182, St Augustine

4 Beds 3 Baths 2,021 SqFt Residential MLS® # 2047534
New
343 Twilight Lane 109, St Augustine

$572,990

343 Twilight Lane 109, St Augustine

4 Beds 3 Baths 2,190 SqFt Residential MLS® # 2047520
New
332 Twilight Lane 28, St Augustine

$612,990

332 Twilight Lane 28, St Augustine

5 Beds 4 Baths 2,853 SqFt Residential MLS® # 2047519
New
88 Whirlwind Place 153, St Augustine

$481,990

88 Whirlwind Place 153, St Augustine

4 Beds 3 Baths 1,968 SqFt Residential MLS® # 2047517
New Pending
320 Whirlwind Place 183, St Augustine

$429,990

320 Whirlwind Place 183, St Augustine

3 Beds 2 Baths 1,613 SqFt Residential MLS® # 2047513
New
724 S Lilac Loop, Jacksonville

$425,000

724 S Lilac Loop, Jacksonville

4 Beds 2 Baths 1,762 SqFt Residential MLS® # 2047491
New
162 Oceanview Drive, St Augustine

$799,000

162 Oceanview Drive, St Augustine

3 Beds 3 Baths 2,050 SqFt Residential MLS® # 2047483
New
14 Lovett Street, St Augustine

$475,000

14 Lovett Street, St Augustine

3 Beds 2 Baths 1,068 SqFt Residential MLS® # 2047473
New
216 Golden Fern Drive, St Augustine

$675,000

216 Golden Fern Drive, St Augustine

4 Beds 3 Baths 2,185 SqFt Residential MLS® # 2047470
New
176 Tamar Court, St Augustine

$407,000

176 Tamar Court, St Augustine

3 Beds 2 Baths 1,388 SqFt Residential MLS® # 2047467

St. John's County Homes With Guest Suite Market Data

St. John's County Homes With Guest Suite housing market statistics: As of September 16, 2024 there are currently 2,659 properties for sale in St. John's County Homes With Guest Suite, with an average asking price of $804,812. The highest-priced property is $12,950,000 and the lowest-priced property can be purchased for $120,000. St. John's County Homes With Guest Suite listings have an average price of $312 per square feet, based on listings with 4 beds, 3 baths, and 2,457 square feet of living space.