--- a/browser/devtools/debugger/debugger-toolbar.js
+++ b/browser/devtools/debugger/debugger-toolbar.js
@@ -1066,31 +1066,37 @@ FilterView.prototype = {
    *        The operator to use for filtering.
    */
   _doSearch: function(aOperator = "", aText = "") {
     this._searchbox.focus();
     this._searchbox.value = ""; // Need to clear value beforehand. Bug 779738.
 
     if (aText) {
       this._searchbox.value = aOperator + aText;
+      return;
     }
-    else if (DebuggerView.editor.somethingSelected()) {
+    if (DebuggerView.editor.somethingSelected()) {
       this._searchbox.value = aOperator + DebuggerView.editor.getSelection();
+      return;
     }
-    else {
+    if (SEARCH_AUTOFILL.indexOf(aOperator) != -1) {
       let cursor = DebuggerView.editor.getCursor();
       let content = DebuggerView.editor.getText();
       let location = DebuggerView.Sources.selectedValue;
       let source = DebuggerController.Parser.get(content, location);
       let identifier = source.getIdentifierAt({ line: cursor.line+1, column: cursor.ch });
 
       if (identifier && identifier.name) {
         this._searchbox.value = aOperator + identifier.name;
+        this._searchbox.select();
+        this._searchbox.selectionStart += aOperator.length;
+        return;
       }
     }
+    this._searchbox.value = aOperator;
   },
 
   /**
    * Called when the source location filter key sequence was pressed.
    */
   _doFileSearch: function() {
     this._doSearch();
     this._searchboxHelpPanel.openPopup(this._searchbox);

--- a/browser/devtools/debugger/debugger-view.js
+++ b/browser/devtools/debugger/debugger-view.js
@@ -21,16 +21,17 @@ const GLOBAL_SEARCH_EXPAND_MAX_RESULTS =
 const GLOBAL_SEARCH_LINE_MAX_LENGTH = 300; // chars
 const GLOBAL_SEARCH_ACTION_MAX_DELAY = 1500; // ms
 const FUNCTION_SEARCH_ACTION_MAX_DELAY = 400; // ms
 const SEARCH_GLOBAL_FLAG = "!";
 const SEARCH_FUNCTION_FLAG = "@";
 const SEARCH_TOKEN_FLAG = "#";
 const SEARCH_LINE_FLAG = ":";
 const SEARCH_VARIABLE_FLAG = "*";
+const SEARCH_AUTOFILL = [SEARCH_GLOBAL_FLAG, SEARCH_FUNCTION_FLAG, SEARCH_TOKEN_FLAG];
 const EDITOR_VARIABLE_HOVER_DELAY = 350; // ms
 const EDITOR_VARIABLE_POPUP_POSITION = "topcenter bottomleft";
 const TOOLBAR_ORDER_POPUP_POSITION = "topcenter bottomleft";
 
 /**
  * Object defining the debugger view components.
  */
 let DebuggerView = {

--- a/browser/devtools/debugger/test/browser.ini
+++ b/browser/devtools/debugger/test/browser.ini
@@ -160,16 +160,17 @@ support-files =
 [browser_dbg_progress-listener-bug.js]
 [browser_dbg_reload-preferred-script-01.js]
 [browser_dbg_reload-preferred-script-02.js]
 [browser_dbg_reload-preferred-script-03.js]
 [browser_dbg_reload-same-script.js]
 [browser_dbg_scripts-switching-01.js]
 [browser_dbg_scripts-switching-02.js]
 [browser_dbg_scripts-switching-03.js]
+[browser_dbg_search-autofill-identifier.js]
 [browser_dbg_search-basic-01.js]
 [browser_dbg_search-basic-02.js]
 [browser_dbg_search-basic-03.js]
 [browser_dbg_search-basic-04.js]
 [browser_dbg_search-global-01.js]
 [browser_dbg_search-global-02.js]
 [browser_dbg_search-global-03.js]
 [browser_dbg_search-global-04.js]
@@ -242,15 +243,14 @@ support-files =
 [browser_dbg_variables-view-popup-07.js]
 [browser_dbg_variables-view-popup-08.js]
 [browser_dbg_variables-view-popup-09.js]
 [browser_dbg_variables-view-reexpand-01.js]
 [browser_dbg_variables-view-reexpand-02.js]
 [browser_dbg_variables-view-webidl.js]
 [browser_dbg_watch-expressions-01.js]
 [browser_dbg_watch-expressions-02.js]
-[browser_dbg_search-function.js]
 [browser_dbg_chrome-create.js]
 skip-if = os == "linux" # Bug 847558
 [browser_dbg_on-pause-raise.js]
 skip-if = os == "linux" # Bug 888811 & bug 891176
 [browser_dbg_break-on-dom-event.js]
 skip-if = os == "mac" # Bug 895426

rename from browser/devtools/debugger/test/browser_dbg_search-function.js
rename to browser/devtools/debugger/test/browser_dbg_search-autofill-identifier.js
--- a/browser/devtools/debugger/test/browser_dbg_search-function.js
+++ b/browser/devtools/debugger/test/browser_dbg_search-autofill-identifier.js
@@ -1,28 +1,135 @@
 /* Any copyright is dedicated to the Public Domain.
    http://creativecommons.org/publicdomain/zero/1.0/ */
 
 /**
- * Tests that Debugger Search uses the identifier under cursor
- * if nothing is selected or manually passed
+ * Tests that Debugger Search uses the identifier under cursor if nothing is
+ * selected or manually passed and searching using certain operators.
  */
-
 "use strict";
 
 function test() {
-
   const TAB_URL = EXAMPLE_URL + "doc_function-search.html";
 
   initDebugger(TAB_URL).then(([aTab, aDebuggee, aPanel]) => {
     let Source = 'code_function-search-01.js';
     let Debugger = aPanel.panelWin;
     let Editor = Debugger.DebuggerView.editor;
     let Filtering = Debugger.DebuggerView.Filtering;
 
+    function doSearch(aOperator) {
+      Editor.dropSelection();
+      Filtering._doSearch(aOperator);
+    }
+
     waitForSourceShown(aPanel, Source).then(() => {
+      info("Testing with cursor at the beginning of the file...");
+
+      doSearch();
+      is(Filtering._searchbox.value, "",
+        "The searchbox value should not be auto-filled when searching for files.");
+      is(Filtering._searchbox.selectionStart, Filtering._searchbox.selectionEnd,
+        "The searchbox contents should not be selected");
+      is(Editor.getSelection(), "",
+        "The selection in the editor should be empty.");
+
+      doSearch("!");
+      is(Filtering._searchbox.value, "!",
+        "The searchbox value should not be auto-filled when searching across all files.");
+      is(Filtering._searchbox.selectionStart, Filtering._searchbox.selectionEnd,
+        "The searchbox contents should not be selected");
+      is(Editor.getSelection(), "",
+        "The selection in the editor should be empty.");
+
+      doSearch("@");
+      is(Filtering._searchbox.value, "@",
+        "The searchbox value should not be auto-filled when searching for functions.");
+      is(Filtering._searchbox.selectionStart, Filtering._searchbox.selectionEnd,
+        "The searchbox contents should not be selected");
+      is(Editor.getSelection(), "",
+        "The selection in the editor should be empty.");
+
+      doSearch("#");
+      is(Filtering._searchbox.value, "#",
+        "The searchbox value should not be auto-filled when searching inside a file.");
+      is(Filtering._searchbox.selectionStart, Filtering._searchbox.selectionEnd,
+        "The searchbox contents should not be selected");
+      is(Editor.getSelection(), "",
+        "The selection in the editor should be empty.");
+
+      doSearch(":");
+      is(Filtering._searchbox.value, ":",
+        "The searchbox value should not be auto-filled when searching for a line.");
+      is(Filtering._searchbox.selectionStart, Filtering._searchbox.selectionEnd,
+        "The searchbox contents should not be selected");
+      is(Editor.getSelection(), "",
+        "The selection in the editor should be empty.");
+
+      doSearch("*");
+      is(Filtering._searchbox.value, "*",
+        "The searchbox value should not be auto-filled when searching for variables.");
+      is(Filtering._searchbox.selectionStart, Filtering._searchbox.selectionEnd,
+        "The searchbox contents should not be selected");
+      is(Editor.getSelection(), "",
+        "The selection in the editor should be empty.");
+
       Editor.setCursor({ line: 7, ch: 0});
-      Filtering._doSearch("@");
-      is(Filtering._searchbox.value, "@test", "Searchbox value should be set to the identifier under cursor if no aText or selection provided");
+      info("Testing with cursor at line 8 and char 1...");
+
+      doSearch();
+      is(Filtering._searchbox.value, "",
+        "The searchbox value should not be auto-filled when searching for files.");
+      is(Filtering._searchbox.selectionStart, Filtering._searchbox.selectionEnd,
+        "The searchbox contents should not be selected");
+      is(Editor.getSelection(), "",
+        "The selection in the editor should be empty.");
+
+      doSearch("!");
+      is(Filtering._searchbox.value, "!test",
+        "The searchbox value was incorrect when searching across all files.");
+      is(Filtering._searchbox.selectionStart, 1,
+        "The searchbox operator should not be selected");
+      is(Filtering._searchbox.selectionEnd, 5,
+        "The searchbox contents should be selected");
+      is(Editor.getSelection(), "",
+        "The selection in the editor should be empty.");
+
+      doSearch("@");
+      is(Filtering._searchbox.value, "@test",
+        "The searchbox value was incorrect when searching for functions.");
+      is(Filtering._searchbox.selectionStart, 1,
+        "The searchbox operator should not be selected");
+      is(Filtering._searchbox.selectionEnd, 5,
+        "The searchbox contents should be selected");
+      is(Editor.getSelection(), "",
+        "The selection in the editor should be empty.");
+
+      doSearch("#");
+      is(Filtering._searchbox.value, "#test",
+        "The searchbox value should be auto-filled when searching inside a file.");
+      is(Filtering._searchbox.selectionStart, 1,
+        "The searchbox operator should not be selected");
+      is(Filtering._searchbox.selectionEnd, 5,
+        "The searchbox contents should be selected");
+      is(Editor.getSelection(), "test",
+        "The selection in the editor should be 'test'.");
+
+      doSearch(":");
+      is(Filtering._searchbox.value, ":",
+        "The searchbox value should not be auto-filled when searching for a line.");
+      is(Filtering._searchbox.selectionStart, Filtering._searchbox.selectionEnd,
+        "The searchbox contents should not be selected");
+      is(Editor.getSelection(), "",
+        "The selection in the editor should be empty.");
+
+      doSearch("*");
+      is(Filtering._searchbox.value, "*",
+        "The searchbox value should not be auto-filled when searching for variables.");
+      is(Filtering._searchbox.selectionStart, Filtering._searchbox.selectionEnd,
+        "The searchbox contents should not be selected");
+      is(Editor.getSelection(), "",
+        "The selection in the editor should be empty.");
+
       closeDebuggerAndFinish(aPanel);
     });
   });
 };