--- a/browser/base/content/test/urlbar/browser.ini
+++ b/browser/base/content/test/urlbar/browser.ini
@@ -68,16 +68,20 @@ support-files =
 skip-if = os == "linux" # Bug 1073339 - Investigate autocomplete test unreliability on Linux/e10s
 [browser_urlbarFocusedCmdK.js]
 [browser_urlbarHashChangeProxyState.js]
 [browser_urlbarKeepStateAcrossTabSwitches.js]
 [browser_urlbarOneOffs.js]
 support-files =
   searchSuggestionEngine.xml
   searchSuggestionEngine.sjs
+[browser_urlbarOneOffs_searchSuggestions.js]
+support-files =
+  searchSuggestionEngine.xml
+  searchSuggestionEngine.sjs
 [browser_urlbarPrivateBrowsingWindowChange.js]
 [browser_urlbarRaceWithTabs.js]
 [browser_urlbarRevert.js]
 [browser_urlbarSearchSingleWordNotification.js]
 [browser_urlbarSearchSuggestions.js]
 support-files =
   searchSuggestionEngine.xml
   searchSuggestionEngine.sjs

--- a/browser/base/content/test/urlbar/browser_urlbarOneOffs.js
+++ b/browser/base/content/test/urlbar/browser_urlbarOneOffs.js
@@ -191,17 +191,17 @@ add_task(async function oneOffClick() {
   let typedValue = "foo.bar";
   await promiseAutocompleteResultPopup(typedValue);
 
   assertState(0, -1, typedValue);
 
   let oneOffs = gURLBar.popup.oneOffSearchButtons.getSelectableButtons(true);
   let resultsPromise =
     BrowserTestUtils.browserLoaded(gBrowser.selectedBrowser, false,
-                                   "http://mochi.test:8888/");
+                                   "http://mochi.test:8888/?terms=foo.bar");
   EventUtils.synthesizeMouseAtCenter(oneOffs[0], {});
   await resultsPromise;
 
   gBrowser.removeTab(gBrowser.selectedTab);
 });
 
 // Presses the Return key when a one-off is selected.
 add_task(async function oneOffReturn() {
@@ -215,17 +215,17 @@ add_task(async function oneOffReturn() {
   assertState(0, -1, typedValue);
 
   // Alt+Down to select the first one-off.
   EventUtils.synthesizeKey("VK_DOWN", { altKey: true })
   assertState(0, 0, typedValue);
 
   let resultsPromise =
     BrowserTestUtils.browserLoaded(gBrowser.selectedBrowser, false,
-                                   "http://mochi.test:8888/");
+                                   "http://mochi.test:8888/?terms=foo.bar");
   EventUtils.synthesizeKey("VK_RETURN", {})
   await resultsPromise;
 
   gBrowser.removeTab(gBrowser.selectedTab);
 });
 
 
 function assertState(result, oneOff, textValue = undefined) {

new file mode 100644
--- /dev/null
+++ b/browser/base/content/test/urlbar/browser_urlbarOneOffs_searchSuggestions.js
@@ -0,0 +1,115 @@
+const TEST_ENGINE_BASENAME = "searchSuggestionEngine.xml";
+
+add_task(async function init() {
+  await PlacesTestUtils.clearHistory();
+  await SpecialPowers.pushPrefEnv({
+    set: [["browser.urlbar.oneOffSearches", true],
+          ["browser.urlbar.suggest.searches", true]],
+  });
+  let engine = await promiseNewSearchEngine(TEST_ENGINE_BASENAME);
+  let oldCurrentEngine = Services.search.currentEngine;
+  Services.search.moveEngine(engine, 0);
+  Services.search.currentEngine = engine;
+  registerCleanupFunction(async function() {
+    Services.search.currentEngine = oldCurrentEngine;
+
+    await PlacesTestUtils.clearHistory();
+    // Make sure the popup is closed for the next test.
+    gURLBar.blur();
+    Assert.ok(!gURLBar.popup.popupOpen, "popup should be closed");
+  });
+});
+
+// Presses the Return key when a one-off is selected after selecting a search
+// suggestion.
+add_task(async function oneOffReturnAfterSuggestion() {
+  let tab = await BrowserTestUtils.openNewForegroundTab(gBrowser);
+
+  let typedValue = "foo";
+  await promiseAutocompleteResultPopup(typedValue, window, true);
+  await BrowserTestUtils.waitForCondition(suggestionsPresent,
+                                          "waiting for suggestions");
+  assertState(0, -1, typedValue);
+
+  // Down to select the first search suggestion.
+  EventUtils.synthesizeKey("VK_DOWN", {})
+  assertState(1, -1, "foofoo");
+
+  // Down to select the next search suggestion.
+  EventUtils.synthesizeKey("VK_DOWN", {})
+  assertState(2, -1, "foobar");
+
+  // Alt+Down to select the first one-off.
+  EventUtils.synthesizeKey("VK_DOWN", { altKey: true })
+  assertState(2, 0, "foobar");
+
+  let resultsPromise =
+    BrowserTestUtils.browserLoaded(gBrowser.selectedBrowser, false,
+                                   `http://mochi.test:8888/?terms=foobar`);
+  EventUtils.synthesizeKey("VK_RETURN", {});
+  await resultsPromise;
+
+  await PlacesTestUtils.clearHistory();
+  await BrowserTestUtils.removeTab(tab);
+});
+
+// Clicks a one-off engine after selecting a search suggestion.
+add_task(async function oneOffClickAfterSuggestion() {
+  let tab = await BrowserTestUtils.openNewForegroundTab(gBrowser);
+
+  let typedValue = "foo";
+  await promiseAutocompleteResultPopup(typedValue, window, true);
+  await BrowserTestUtils.waitForCondition(suggestionsPresent,
+                                          "waiting for suggestions");
+  assertState(0, -1, typedValue);
+
+  // Down to select the first search suggestion.
+  EventUtils.synthesizeKey("VK_DOWN", {})
+  assertState(1, -1, "foofoo");
+
+  // Down to select the next search suggestion.
+  EventUtils.synthesizeKey("VK_DOWN", {})
+  assertState(2, -1, "foobar");
+
+  let oneOffs = gURLBar.popup.oneOffSearchButtons.getSelectableButtons(true);
+  let resultsPromise =
+    BrowserTestUtils.browserLoaded(gBrowser.selectedBrowser, false,
+                                   `http://mochi.test:8888/?terms=foobar`);
+  EventUtils.synthesizeMouseAtCenter(oneOffs[0], {});
+  await resultsPromise;
+
+  await PlacesTestUtils.clearHistory();
+  await BrowserTestUtils.removeTab(tab);
+});
+
+function assertState(result, oneOff, textValue = undefined) {
+  Assert.equal(gURLBar.popup.selectedIndex, result,
+               "Expected result should be selected");
+  Assert.equal(gURLBar.popup.oneOffSearchButtons.selectedButtonIndex, oneOff,
+               "Expected one-off should be selected");
+  if (textValue !== undefined) {
+    Assert.equal(gURLBar.textValue, textValue, "Expected textValue");
+  }
+}
+
+async function hidePopup() {
+  EventUtils.synthesizeKey("VK_ESCAPE", {});
+  await promisePopupHidden(gURLBar.popup);
+}
+
+function suggestionsPresent() {
+  let controller = gURLBar.popup.input.controller;
+  let matchCount = controller.matchCount;
+  for (let i = 0; i < matchCount; i++) {
+    let url = controller.getValueAt(i);
+    let mozActionMatch = url.match(/^moz-action:([^,]+),(.*)$/);
+    if (mozActionMatch) {
+      let [, type, paramStr] = mozActionMatch;
+      let params = JSON.parse(paramStr);
+      if (type == "searchengine" && "searchSuggestion" in params) {
+        return true;
+      }
+    }
+  }
+  return false;
+}

--- a/browser/base/content/test/urlbar/searchSuggestionEngine.xml
+++ b/browser/base/content/test/urlbar/searchSuggestionEngine.xml
@@ -1,9 +1,11 @@
 <?xml version="1.0" encoding="UTF-8"?>
 <!-- Any copyright is dedicated to the Public Domain.
    - http://creativecommons.org/publicdomain/zero/1.0/ -->
 
 <SearchPlugin xmlns="http://www.mozilla.org/2006/browser/search/">
 <ShortName>browser_searchSuggestionEngine searchSuggestionEngine.xml</ShortName>
 <Url type="application/x-suggestions+json" method="GET" template="http://mochi.test:8888/browser/browser/base/content/test/urlbar/searchSuggestionEngine.sjs?{searchTerms}"/>
-<Url type="text/html" method="GET" template="http://mochi.test:8888/" rel="searchform"/>
+<Url type="text/html" method="GET" template="http://mochi.test:8888/" rel="searchform">
+  <Param name="terms" value="{searchTerms}"/>
+</Url>
 </SearchPlugin>

--- a/browser/base/content/urlbarBindings.xml
+++ b/browser/base/content/urlbarBindings.xml
@@ -666,16 +666,23 @@ file, You can obtain one at http://mozil
 
           this._loadURL(url, browser, postData, where, openUILinkParams,
                         mayInheritPrincipal);
         ]]></body>
       </method>
 
       <property name="oneOffSearchQuery">
         <getter><![CDATA[
+          // If the user has selected a search suggestion, chances are they
+          // want to use the one off search engine to search for that suggestion,
+          // not the string that they manually entered into the location bar.
+          let action = this._parseActionUrl(this.value);
+          if (action && action.type == "searchengine") {
+            return action.params.input;
+          }
           // this.textValue may be an autofilled string.  Search only with the
           // portion that the user typed, if any, by preferring the autocomplete
           // controller's searchString (including handleEnterInstance.searchString).
           return this.handleEnterSearchString ||
                  this.mController.searchString ||
                  this.textValue;
         ]]></getter>
       </property>