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
165 Edgewater Branch Dr, ST JOHNS

$590,000

165 Edgewater Branch Dr, ST JOHNS

4 Beds 2 Baths 2,258 SqFt Residential MLS® # 1259182
New
24298 Marsh Landing Pkwy, PONTE VEDRA BEACH

$950,000

24298 Marsh Landing Pkwy, PONTE VEDRA BEACH

3 Beds 3 Baths 1,893 SqFt Residential MLS® # 1259250
New
655 Cedar Preserve Ln, ST AUGUSTINE

$721,890

655 Cedar Preserve Ln, ST AUGUSTINE

5 Beds 5 Baths 3,459 SqFt Residential MLS® # 1259149
New Pending
530 Palm Crest Dr, PONTE VEDRA

$1,013,849

530 Palm Crest Dr, PONTE VEDRA

3 Beds 4 Baths 2,989 SqFt Residential MLS® # 1259076
345 Redwing Ln, ST AUGUSTINE

$1,530,000

345 Redwing Ln, ST AUGUSTINE

4 Beds 4 Baths 2,918 SqFt Residential MLS® # 1258851
1605 Merroway Ln, PONTE VEDRA

$615,000

1605 Merroway Ln, PONTE VEDRA

5 Beds 4 Baths 2,649 SqFt Residential MLS® # 1257996
411 Pantano Dr, ST AUGUSTINE

$973,500

411 Pantano Dr, ST AUGUSTINE

4 Beds 3 Baths 2,750 SqFt Residential MLS® # 1244188
407 N Landguard Rd, ST AUGUSTINE

$675,000

407 N Landguard Rd, ST AUGUSTINE

4 Beds 3 Baths 2,981 SqFt Residential MLS® # 1258620
381 County Road 13 S, ST AUGUSTINE

$999,000

381 County Road 13 S, ST AUGUSTINE

3 Beds 3 Baths 2,168 SqFt Residential MLS® # 1258326
129 Daniel Creek Ct, ST AUGUSTINE

$499,900

129 Daniel Creek Ct, ST AUGUSTINE

4 Beds 3 Baths 2,398 SqFt Residential MLS® # 1258592
Under Contract
2435 Den St, ST AUGUSTINE

$989,500

2435 Den St, ST AUGUSTINE

4 Beds 3 Baths 3,230 SqFt Residential MLS® # 1258556
165 Storybrook Point, PONTE VEDRA

$1,313,222

165 Storybrook Point, PONTE VEDRA

5 Beds 6 Baths 3,726 SqFt Residential MLS® # 1258497
387 Meadow Ridge Dr, ST AUGUSTINE

$569,900

387 Meadow Ridge Dr, ST AUGUSTINE

4 Beds 3 Baths 2,498 SqFt Residential MLS® # 1258281
1408 S Burgandy Trl, ST JOHNS

$689,000

↓ $36,000

1408 S Burgandy Trl, ST JOHNS

5 Beds 4 Baths 2,914 SqFt Residential MLS® # 1256688
156 Morgan Ave, ST AUGUSTINE

$1,948,730

156 Morgan Ave, ST AUGUSTINE

4 Beds 3 Baths 3,113 SqFt Residential MLS® # 1257975
239 Blue Cypress Trl, ST AUGUSTINE

$477,394

↑ $4,009

239 Blue Cypress Trl, ST AUGUSTINE

4 Beds 3 Baths 2,695 SqFt Residential MLS® # 1257985
795 Old Bluff Dr, PONTE VEDRA

$1,800,000

795 Old Bluff Dr, PONTE VEDRA

5 Beds 5 Baths 4,359 SqFt Residential MLS® # 1257023
24617 Harbour View Dr, PONTE VEDRA BEACH

$3,250,000

24617 Harbour View Dr, PONTE VEDRA BEACH

5 Beds 8 Baths 7,298 SqFt Residential MLS® # 1257733
118 Surrey Ln, PONTE VEDRA BEACH

$2,200,000

118 Surrey Ln, PONTE VEDRA BEACH

4 Beds 4 Baths 3,054 SqFt Residential MLS® # 1257479
Pending
470 Seagrove Dr, PONTE VEDRA

$1,227,636

470 Seagrove Dr, PONTE VEDRA

5 Beds 4 Baths 3,435 SqFt Residential MLS® # 1257311
Pending
196 Seagrove Dr, PONTE VEDRA

$1,417,502

196 Seagrove Dr, PONTE VEDRA

5 Beds 6 Baths 4,300 SqFt Residential MLS® # 1257309
Pending
616 Seagrove Dr, PONTE VEDRA

$1,233,770

616 Seagrove Dr, PONTE VEDRA

4 Beds 5 Baths 4,300 SqFt Residential MLS® # 1257276
Pending
658 Seagrove Dr, PONTE VEDRA

$1,242,885

658 Seagrove Dr, PONTE VEDRA

5 Beds 6 Baths 4,327 SqFt Residential MLS® # 1257274
Pending
475 Seagrove Dr, PONTE VEDRA

$1,185,508

475 Seagrove Dr, PONTE VEDRA

4 Beds 5 Baths 4,277 SqFt Residential MLS® # 1257271

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

St. John's County Homes With Guest Suite housing market statistics: As of December 4, 2023 there are currently 136 properties for sale in St. John's County Homes With Guest Suite, with an average asking price of $1,284,130. The highest-priced property is $8,995,000 and the lowest-priced property can be purchased for $450,000. St. John's County Homes With Guest Suite listings have an average price of $366 per square feet, based on listings with 4 beds, 4 baths, and 3,287 square feet of living space.