diff --git a/CHANGELOG.md b/CHANGELOG.md
index 7c1e99ef036..91e2399181f 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -13,6 +13,7 @@
 - Fixed `euiBreakpoint()` warning to give accurate feedback ([#1874](https://github.com/elastic/eui/pull/1874))
 - Fixed type definitions around `EuiI18n`'s `default` prop to better support use cases ([#1861](https://github.com/elastic/eui/pull/1861))
 - Localized `EuiTablePagination`'s row count selection ([#1883](https://github.com/elastic/eui/pull/1883))
+- Fixed EuiComboBox's internal tracking of its focus state ([#1796](https://github.com/elastic/eui/pull/1796))
 - Fixed `EuiComboBox` with `singleSelection` and `onAddCustomOption` reopening the options list after adding a custom option ([#1882](https://github.com/elastic/eui/pull/1882))
 - Fixed `EuiComboBox` reopening the options list in Firefox when closing via the dropdown arrow button ([#1885](https://github.com/elastic/eui/pull/1885))
 
diff --git a/src-docs/src/views/combo_box/disallow_custom_options.js b/src-docs/src/views/combo_box/disallow_custom_options.js
index f3448ac5c0e..da625e06213 100644
--- a/src-docs/src/views/combo_box/disallow_custom_options.js
+++ b/src-docs/src/views/combo_box/disallow_custom_options.js
@@ -2,6 +2,7 @@ import React, { Component } from 'react';
 
 import {
   EuiComboBox,
+  EuiFormRow,
 } from '../../../../src/components';
 
 export default class extends Component {
@@ -32,24 +33,46 @@ export default class extends Component {
     }];
 
     this.state = {
+      error: undefined,
       selectedOptions: [this.options[2], this.options[4]],
     };
   }
 
   onChange = (selectedOptions) => {
     this.setState({
+      error: undefined,
       selectedOptions,
     });
-  };
+  }
+
+  onSearchChange = (value, hasMatchingOptions) => {
+    this.setState({
+      error: value.length === 0 || hasMatchingOptions ? undefined : `"${value}" is not a valid option`,
+    });
+  }
+
+  onBlur = () => {
+    const { value } = this.inputRef;
+    this.setState({
+      error: value.length === 0 ? undefined : `"${value}" is not a valid option`,
+    });
+  }
+
+  setInputRef = ref => this.inputRef = ref;
 
   render() {
     return (
-      <EuiComboBox
-        placeholder="Select from a list of options"
-        options={this.options}
-        selectedOptions={this.state.selectedOptions}
-        onChange={this.onChange}
-      />
+      <EuiFormRow error={this.state.error} isInvalid={this.state.error !== undefined}>
+        <EuiComboBox
+          placeholder="Select from a list of options"
+          options={this.options}
+          selectedOptions={this.state.selectedOptions}
+          inputRef={this.setInputRef}
+          onChange={this.onChange}
+          onSearchChange={this.onSearchChange}
+          onBlur={this.onBlur}
+        />
+      </EuiFormRow>
     );
   }
 }
diff --git a/src/components/combo_box/__snapshots__/combo_box.test.js.snap b/src/components/combo_box/__snapshots__/combo_box.test.js.snap
index d81d523c000..87119129568 100644
--- a/src/components/combo_box/__snapshots__/combo_box.test.js.snap
+++ b/src/components/combo_box/__snapshots__/combo_box.test.js.snap
@@ -89,7 +89,6 @@ exports[`props full width is rendered 1`] = `
     inputRef={[Function]}
     isListOpen={false}
     noIcon={false}
-    onBlur={[Function]}
     onChange={[Function]}
     onClear={[Function]}
     onClick={[Function]}
@@ -131,7 +130,6 @@ exports[`props isClearable=false disallows user from clearing input when no opti
     inputRef={[Function]}
     isListOpen={false}
     noIcon={false}
-    onBlur={[Function]}
     onChange={[Function]}
     onClick={[Function]}
     onCloseListClick={[Function]}
@@ -166,7 +164,6 @@ exports[`props isClearable=false disallows user from clearing input when options
     inputRef={[Function]}
     isListOpen={false}
     noIcon={false}
-    onBlur={[Function]}
     onChange={[Function]}
     onClick={[Function]}
     onCloseListClick={[Function]}
@@ -211,7 +208,6 @@ exports[`props isDisabled is rendered 1`] = `
     isDisabled={true}
     isListOpen={false}
     noIcon={false}
-    onBlur={[Function]}
     onChange={[Function]}
     onClick={[Function]}
     onCloseListClick={[Function]}
@@ -342,7 +338,6 @@ exports[`props selectedOptions are rendered 1`] = `
     inputRef={[Function]}
     isListOpen={false}
     noIcon={false}
-    onBlur={[Function]}
     onChange={[Function]}
     onClear={[Function]}
     onClick={[Function]}
@@ -387,7 +382,6 @@ exports[`props singleSelection is rendered 1`] = `
     inputRef={[Function]}
     isListOpen={false}
     noIcon={false}
-    onBlur={[Function]}
     onChange={[Function]}
     onClear={[Function]}
     onClick={[Function]}
@@ -429,7 +423,6 @@ exports[`props singleSelection selects existing option when opened 1`] = `
     inputRef={[Function]}
     isListOpen={true}
     noIcon={false}
-    onBlur={[Function]}
     onChange={[Function]}
     onClear={[Function]}
     onClick={[Function]}
diff --git a/src/components/combo_box/combo_box.js b/src/components/combo_box/combo_box.js
index 405f28ce1a7..9e438515c43 100644
--- a/src/components/combo_box/combo_box.js
+++ b/src/components/combo_box/combo_box.js
@@ -314,6 +314,7 @@ export class EuiComboBox extends Component {
       if (this.props.onBlur) {
         this.props.onBlur();
       }
+      this.setState({ hasFocus: false });
 
       // If the user tabs away or changes focus to another element, take whatever input they've
       // typed and convert it into a pill, to prevent the combo box from looking like a text input.
@@ -323,10 +324,6 @@ export class EuiComboBox extends Component {
     }
   }
 
-  onComboBoxBlur = () => {
-    this.setState({ hasFocus: false });
-  }
-
   onKeyDown = (e) => {
     switch (e.keyCode) {
       case comboBoxKeyCodes.UP:
@@ -457,7 +454,8 @@ export class EuiComboBox extends Component {
 
   onSearchChange = (searchValue) => {
     if (this.props.onSearchChange) {
-      this.props.onSearchChange(searchValue);
+      const hasMatchingOptions = this.state.matchingOptions.length > 0;
+      this.props.onSearchChange(searchValue, hasMatchingOptions);
     }
 
     this.setState(
@@ -616,7 +614,10 @@ export class EuiComboBox extends Component {
     } = this.props;
     const { hasFocus, searchValue, isListOpen, listPosition, width, activeOptionIndex } = this.state;
 
-    const markAsInvalid = isInvalid || (hasFocus === false && searchValue);
+    // Visually indicate the combobox is in an invalid state if it has lost focus but there is text entered in the input.
+    // When custom options are disabled and the user leaves the combo box after entering text that does not match any
+    // options, this tells the user that they've entered invalid input.
+    const markAsInvalid = isInvalid || ((hasFocus === false || isListOpen === false) && searchValue);
 
     const classes = classNames('euiComboBox', className, {
       'euiComboBox-isOpen': isListOpen,
@@ -679,7 +680,6 @@ export class EuiComboBox extends Component {
           placeholder={placeholder}
           selectedOptions={selectedOptions}
           onRemoveOption={this.onRemoveOption}
-          onBlur={this.onComboBoxBlur}
           onClick={this.onComboBoxClick}
           onChange={this.onSearchChange}
           onFocus={this.onComboBoxFocus}