--- a/browser/devtools/framework/toolbox.js
+++ b/browser/devtools/framework/toolbox.js
@@ -259,26 +259,29 @@ Toolbox.prototype = {
         this._loadInitialZoom();
 
         this.webconsolePanel = this.doc.querySelector("#toolbox-panel-webconsole");
         this.webconsolePanel.height =
           Services.prefs.getIntPref(SPLITCONSOLE_HEIGHT_PREF);
         this.webconsolePanel.addEventListener("resize",
           this._saveSplitConsoleHeight);
 
-        let splitConsolePromise = promise.resolve();
-        if (Services.prefs.getBoolPref(SPLITCONSOLE_ENABLED_PREF)) {
-          splitConsolePromise = this.openSplitConsole();
-        }
-
         let buttonsPromise = this._buildButtons();
 
         this._telemetry.toolOpened("toolbox");
 
         this.selectTool(this._defaultToolId).then(panel => {
+
+          // Wait until the original tool is selected so that the split
+          // console input will receive focus.
+          let splitConsolePromise = promise.resolve();
+          if (Services.prefs.getBoolPref(SPLITCONSOLE_ENABLED_PREF)) {
+            splitConsolePromise = this.openSplitConsole();
+          }
+
           promise.all([
             splitConsolePromise,
             buttonsPromise
           ]).then(() => {
             this.emit("ready");
             deferred.resolve();
           }, deferred.reject);
         });
@@ -974,19 +977,19 @@ Toolbox.prototype = {
     let iframe = this.doc.getElementById("toolbox-panel-iframe-" + id);
     iframe.focus();
   },
 
   /**
    * Focus split console's input line
    */
   focusConsoleInput: function() {
-    let hud = this.getPanel("webconsole").hud;
-    if (hud && hud.jsterm) {
-      hud.jsterm.inputNode.focus();
+    let consolePanel = this.getPanel("webconsole");
+    if (consolePanel) {
+      consolePanel.focusInput();
     }
   },
 
   /**
    * If the console is split and we are focusing an element outside
    * of the console, then store the newly focused element, so that
    * it can be restored once the split console closes.
    */

--- a/browser/devtools/webconsole/test/browser_webconsole_split_persist.js
+++ b/browser/devtools/webconsole/test/browser_webconsole_split_persist.js
@@ -30,16 +30,22 @@ function test() {
     info("Opening a tab while there is a true user setting on split console pref");
     let {tab} = yield loadTab(TEST_URI);
     let target = TargetFactory.forTab(tab);
     toolbox = yield gDevTools.showToolbox(target, "inspector");
 
     ok(toolbox.splitConsole, "Split console is visible by default.");
     is(getHeightPrefValue(), 200, "Height is set based on panel height after closing");
 
+    // Use the binding element since jsterm.inputNode is a XUL textarea element.
+    let activeElement = getActiveElement(toolbox.doc);
+    activeElement = activeElement.ownerDocument.getBindingParent(activeElement);
+    let inputNode = toolbox.getPanel("webconsole").hud.jsterm.inputNode;
+    is(activeElement, inputNode, "Split console input is focused by default");
+
     toolbox.webconsolePanel.height = 1;
     ok (toolbox.webconsolePanel.clientHeight > 1,
         "The actual height of the console is bound with a min height");
 
     toolbox.webconsolePanel.height = 10000;
     ok (toolbox.webconsolePanel.clientHeight < 10000,
         "The actual height of the console is bound with a max height");
 
@@ -58,16 +64,24 @@ function test() {
     toolbox = yield gDevTools.showToolbox(target, "inspector");
 
     ok(!toolbox.splitConsole, "Split console is hidden by default.");
     ok(!getVisiblePrefValue(), "Visibility pref is false");
 
     yield toolbox.destroy();
   }
 
+  function getActiveElement(doc) {
+    let activeElement = doc.activeElement;
+    while (activeElement && activeElement.contentDocument) {
+      activeElement = activeElement.contentDocument.activeElement;
+    }
+    return activeElement;
+  }
+
   function getVisiblePrefValue() {
     return Services.prefs.getBoolPref("devtools.toolbox.splitconsoleEnabled");
   }
 
   function getHeightPrefValue() {
     return Services.prefs.getIntPref("devtools.toolbox.splitconsoleHeight");
   }