diff --git a/src/registrar/assets/js/uswds-edited.js b/src/registrar/assets/js/uswds-edited.js
index f59417b41..9d4dd2e51 100644
--- a/src/registrar/assets/js/uswds-edited.js
+++ b/src/registrar/assets/js/uswds-edited.js
@@ -29,6 +29,7 @@
  *  - tooltip dynamic content updated to include nested element (for better sizing control)
  *  - modal exposed to window to be accessible in other js files
  *  - fixed bug in createHeaderButton which added newlines to header button tooltips
+ *  - modified combobox to handle error class
  */
 
 if ("document" in window.self) {
@@ -1213,6 +1214,11 @@ const enhanceComboBox = _comboBoxEl => {
   input.setAttribute("class", INPUT_CLASS);
   input.setAttribute("type", "text");
   input.setAttribute("role", "combobox");
+  // DOTGOV - handle error class for combobox
+  // Check if 'usa-input--error' exists in selectEl and add it to input if true
+  if (selectEl.classList.contains('usa-input--error')) {
+    input.classList.add('usa-input--error');
+  }
   additionalAttributes.forEach(attr => Object.keys(attr).forEach(key => {
     const value = Sanitizer.escapeHTML`${attr[key]}`;
     input.setAttribute(key, value);
diff --git a/src/registrar/assets/src/js/getgov/combobox.js b/src/registrar/assets/src/js/getgov/combobox.js
deleted file mode 100644
index 36b7aa0ad..000000000
--- a/src/registrar/assets/src/js/getgov/combobox.js
+++ /dev/null
@@ -1,113 +0,0 @@
-import { hideElement, showElement } from './helpers.js';
-
-export function loadInitialValuesForComboBoxes() {
-  var overrideDefaultClearButton = true;
-  var isTyping = false;
-
-  document.addEventListener('DOMContentLoaded', (event) => {
-    handleAllComboBoxElements();
-  });
-
-  function handleAllComboBoxElements() {
-    const comboBoxElements = document.querySelectorAll(".usa-combo-box");
-    comboBoxElements.forEach(comboBox => {
-      const input = comboBox.querySelector("input");
-      const select = comboBox.querySelector("select");
-      if (!input || !select) {
-        console.warn("No combobox element found");
-        return;
-      }
-      // Set the initial value of the combobox
-      let initialValue = select.getAttribute("data-default-value");
-      let clearInputButton = comboBox.querySelector(".usa-combo-box__clear-input");
-      if (!clearInputButton) {
-        console.warn("No clear element found");
-        return;
-      }
-
-      // Override the default clear button behavior such that it no longer clears the input,
-      // it just resets to the data-initial-value.
-      // Due to the nature of how uswds works, this is slightly hacky.
-      // Use a MutationObserver to watch for changes in the dropdown list
-      const dropdownList = comboBox.querySelector(`#${input.id}--list`);
-      const observer = new MutationObserver(function(mutations) {
-          mutations.forEach(function(mutation) {
-              if (mutation.type === "childList") {
-                addBlankOption(clearInputButton, dropdownList, initialValue);
-              }
-          });
-      });
-
-      // Configure the observer to watch for changes in the dropdown list
-      const config = { childList: true, subtree: true };
-      observer.observe(dropdownList, config);
-
-      // Input event listener to detect typing
-      input.addEventListener("input", () => {
-        isTyping = true;
-      });
-
-      // Blur event listener to reset typing state
-      input.addEventListener("blur", () => {
-        isTyping = false;
-      });
-
-      // Hide the reset button when there is nothing to reset.
-      // Do this once on init, then everytime a change occurs.
-      updateClearButtonVisibility(select, initialValue, clearInputButton)
-      select.addEventListener("change", () => {
-        updateClearButtonVisibility(select, initialValue, clearInputButton)
-      });
-
-      // Change the default input behaviour - have it reset to the data default instead
-      clearInputButton.addEventListener("click", (e) => {
-        if (overrideDefaultClearButton && initialValue) {
-          e.preventDefault();
-          e.stopPropagation();
-          input.click();
-          // Find the dropdown option with the desired value
-          const dropdownOptions = document.querySelectorAll(".usa-combo-box__list-option");
-          if (dropdownOptions) {
-            dropdownOptions.forEach(option => {
-                if (option.getAttribute("data-value") === initialValue) {
-                    // Simulate a click event on the dropdown option
-                    option.click();
-                }
-            });
-          }
-        }
-      });
-    });
-  }
-
-  function updateClearButtonVisibility(select, initialValue, clearInputButton) {
-    if (select.value === initialValue) {
-      hideElement(clearInputButton);
-    }else {
-      showElement(clearInputButton)
-    }
-  }
-
-  function addBlankOption(clearInputButton, dropdownList, initialValue) {
-    if (dropdownList && !dropdownList.querySelector('[data-value=""]') && !isTyping) {
-        const blankOption = document.createElement("li");
-        blankOption.setAttribute("role", "option");
-        blankOption.setAttribute("data-value", "");
-        blankOption.classList.add("usa-combo-box__list-option");
-        if (!initialValue){
-          blankOption.classList.add("usa-combo-box__list-option--selected")
-        }
-        blankOption.textContent = "⎯";
-
-        dropdownList.insertBefore(blankOption, dropdownList.firstChild);
-        blankOption.addEventListener("click", (e) => {
-          e.preventDefault();
-          e.stopPropagation();
-          overrideDefaultClearButton = false;
-          // Trigger the default clear behavior
-          clearInputButton.click();
-          overrideDefaultClearButton = true;
-        });
-    }
-  }
-}
diff --git a/src/registrar/assets/src/js/getgov/main.js b/src/registrar/assets/src/js/getgov/main.js
index 6ff402aa4..a077da929 100644
--- a/src/registrar/assets/src/js/getgov/main.js
+++ b/src/registrar/assets/src/js/getgov/main.js
@@ -3,7 +3,6 @@ import { initDomainValidators } from './domain-validators.js';
 import { initFormsetsForms, triggerModalOnDsDataForm, nameserversFormListener } from './formset-forms.js';
 import { initializeUrbanizationToggle } from './urbanization.js';
 import { userProfileListener, finishUserSetupListener } from './user-profile.js';
-import { loadInitialValuesForComboBoxes } from './combobox.js';
 import { handleRequestingEntityFieldset } from './requesting-entity.js';
 import { initDomainsTable } from './table-domains.js';
 import { initDomainRequestsTable } from './table-domain-requests.js';
@@ -31,8 +30,6 @@ initializeUrbanizationToggle();
 userProfileListener();
 finishUserSetupListener();
 
-loadInitialValuesForComboBoxes();
-
 handleRequestingEntityFieldset();
 
 initDomainsTable();
diff --git a/src/registrar/assets/src/js/getgov/requesting-entity.js b/src/registrar/assets/src/js/getgov/requesting-entity.js
index 3bcdcd35c..833eab2f8 100644
--- a/src/registrar/assets/src/js/getgov/requesting-entity.js
+++ b/src/registrar/assets/src/js/getgov/requesting-entity.js
@@ -9,15 +9,15 @@ export function handleRequestingEntityFieldset() {
     const formPrefix = "portfolio_requesting_entity";
     const radioFieldset = document.getElementById(`id_${formPrefix}-requesting_entity_is_suborganization__fieldset`);
     const radios = radioFieldset?.querySelectorAll(`input[name="${formPrefix}-requesting_entity_is_suborganization"]`);
-    const select = document.getElementById(`id_${formPrefix}-sub_organization`);
-    const selectParent = select?.parentElement;
+    const input = document.getElementById(`id_${formPrefix}-sub_organization`);
+    const inputGrandParent = input?.parentElement?.parentElement;
+    const select = input?.previousElementSibling;
     const suborgContainer = document.getElementById("suborganization-container");
     const suborgDetailsContainer = document.getElementById("suborganization-container__details");
     const suborgAddtlInstruction = document.getElementById("suborganization-addtl-instruction");
-    const subOrgCreateNewOption = document.getElementById("option-to-add-suborg")?.value;
     // Make sure all crucial page elements exist before proceeding.
     // This more or less ensures that we are on the Requesting Entity page, and not elsewhere.
-    if (!radios || !select || !selectParent || !suborgContainer || !suborgDetailsContainer) return;
+    if (!radios || !input || !select || !inputGrandParent || !suborgContainer || !suborgDetailsContainer) return;
 
     // requestingSuborganization: This just broadly determines if they're requesting a suborg at all
     // requestingNewSuborganization: This variable determines if the user is trying to *create* a new suborganization or not.
@@ -27,8 +27,8 @@ export function handleRequestingEntityFieldset() {
     function toggleSuborganization(radio=null) {
         if (radio != null) requestingSuborganization = radio?.checked && radio.value === "True";
         requestingSuborganization ? showElement(suborgContainer) : hideElement(suborgContainer);
-        if (select.options.length == 2) { // --Select-- and other are the only options
-            hideElement(selectParent); // Hide the select drop down and indicate requesting new suborg
+        if (select.options.length == 1) { // other is the only option
+            hideElement(inputGrandParent); // Hide the combo box and indicate requesting new suborg
             hideElement(suborgAddtlInstruction); // Hide additional instruction related to the list
             requestingNewSuborganization.value = "True";
         } else {
@@ -37,11 +37,6 @@ export function handleRequestingEntityFieldset() {
         requestingNewSuborganization.value === "True" ? showElement(suborgDetailsContainer) : hideElement(suborgDetailsContainer);
     }
 
-    // Add fake "other" option to sub_organization select
-    if (select && !Array.from(select.options).some(option => option.value === "other")) {
-        select.add(new Option(subOrgCreateNewOption, "other"));
-    }
-
     if (requestingNewSuborganization.value === "True") {
         select.value = "other";
     }
diff --git a/src/registrar/forms/domain.py b/src/registrar/forms/domain.py
index 699efe63b..5eeae232d 100644
--- a/src/registrar/forms/domain.py
+++ b/src/registrar/forms/domain.py
@@ -4,6 +4,7 @@
 from django import forms
 from django.core.validators import MinValueValidator, MaxValueValidator, RegexValidator, MaxLengthValidator
 from django.forms import formset_factory
+from registrar.forms.utility.combobox import ComboboxWidget
 from registrar.models import DomainRequest, FederalAgency
 from phonenumber_field.widgets import RegionalPhoneNumberWidget
 from registrar.models.suborganization import Suborganization
@@ -161,9 +162,11 @@ class DomainSuborganizationForm(forms.ModelForm):
     """Form for updating the suborganization"""
 
     sub_organization = forms.ModelChoiceField(
+        label="Suborganization name",
         queryset=Suborganization.objects.none(),
+        empty_label="⎯ (No suborganization)",
         required=False,
-        widget=forms.Select(),
+        widget=ComboboxWidget,
     )
 
     class Meta:
@@ -178,20 +181,6 @@ def __init__(self, *args, **kwargs):
         portfolio = self.instance.portfolio if self.instance else None
         self.fields["sub_organization"].queryset = Suborganization.objects.filter(portfolio=portfolio)
 
-        # Set initial value
-        if self.instance and self.instance.sub_organization:
-            self.fields["sub_organization"].initial = self.instance.sub_organization
-
-        # Set custom form label
-        self.fields["sub_organization"].label = "Suborganization name"
-
-        # Use the combobox rather than the regular select widget
-        self.fields["sub_organization"].widget.template_name = "django/forms/widgets/combobox.html"
-
-        # Set data-default-value attribute
-        if self.instance and self.instance.sub_organization:
-            self.fields["sub_organization"].widget.attrs["data-default-value"] = self.instance.sub_organization.pk
-
 
 class BaseNameserverFormset(forms.BaseFormSet):
     def clean(self):
@@ -456,6 +445,13 @@ class DomainSecurityEmailForm(forms.Form):
 class DomainOrgNameAddressForm(forms.ModelForm):
     """Form for updating the organization name and mailing address."""
 
+    # for federal agencies we also want to know the top-level agency.
+    federal_agency = forms.ModelChoiceField(
+        label="Federal agency",
+        required=False,
+        queryset=FederalAgency.objects.all(),
+        widget=ComboboxWidget,
+    )
     zipcode = forms.CharField(
         label="Zip code",
         validators=[
@@ -469,6 +465,16 @@ class DomainOrgNameAddressForm(forms.ModelForm):
         },
     )
 
+    state_territory = forms.ChoiceField(
+        label="State, territory, or military post",
+        required=True,
+        choices=DomainInformation.StateTerritoryChoices.choices,
+        error_messages={
+            "required": ("Select the state, territory, or military post where your organization is located.")
+        },
+        widget=ComboboxWidget(),
+    )
+
     class Meta:
         model = DomainInformation
         fields = [
@@ -486,25 +492,12 @@ class Meta:
             "organization_name": {"required": "Enter the name of your organization."},
             "address_line1": {"required": "Enter the street address of your organization."},
             "city": {"required": "Enter the city where your organization is located."},
-            "state_territory": {
-                "required": "Select the state, territory, or military post where your organization is located."
-            },
         }
         widgets = {
-            # We need to set the required attributed for State/territory
-            # because for this fields we are creating an individual
-            # instance of the Select. For the other fields we use the for loop to set
-            # the class's required attribute to true.
             "organization_name": forms.TextInput,
             "address_line1": forms.TextInput,
             "address_line2": forms.TextInput,
             "city": forms.TextInput,
-            "state_territory": forms.Select(
-                attrs={
-                    "required": True,
-                },
-                choices=DomainInformation.StateTerritoryChoices.choices,
-            ),
             "urbanization": forms.TextInput,
         }
 
diff --git a/src/registrar/forms/domain_request_wizard.py b/src/registrar/forms/domain_request_wizard.py
index ccdbb17ba..7c9dcb180 100644
--- a/src/registrar/forms/domain_request_wizard.py
+++ b/src/registrar/forms/domain_request_wizard.py
@@ -7,6 +7,7 @@
 from django.core.validators import RegexValidator, MaxLengthValidator
 from django.utils.safestring import mark_safe
 
+from registrar.forms.utility.combobox import ComboboxWidget
 from registrar.forms.utility.wizard_form_helper import (
     RegistrarForm,
     RegistrarFormSet,
@@ -43,7 +44,7 @@ class RequestingEntityForm(RegistrarForm):
         label="Suborganization name",
         required=False,
         queryset=Suborganization.objects.none(),
-        empty_label="--Select--",
+        widget=ComboboxWidget,
     )
     requested_suborganization = forms.CharField(
         label="Requested suborganization",
@@ -56,22 +57,44 @@ class RequestingEntityForm(RegistrarForm):
     suborganization_state_territory = forms.ChoiceField(
         label="State, territory, or military post",
         required=False,
-        choices=[("", "--Select--")] + DomainRequest.StateTerritoryChoices.choices,
+        choices=DomainRequest.StateTerritoryChoices.choices,
+        widget=ComboboxWidget,
     )
 
     def __init__(self, *args, **kwargs):
-        """Override of init to add the suborganization queryset"""
+        """Override of init to add the suborganization queryset and 'other' option"""
         super().__init__(*args, **kwargs)
 
         if self.domain_request.portfolio:
-            self.fields["sub_organization"].queryset = Suborganization.objects.filter(
-                portfolio=self.domain_request.portfolio
-            )
+            # Fetch the queryset for the portfolio
+            queryset = Suborganization.objects.filter(portfolio=self.domain_request.portfolio)
+            # set the queryset appropriately so that post can validate against queryset
+            self.fields["sub_organization"].queryset = queryset
+
+            # Modify the choices to include "other" so that form can display options properly
+            self.fields["sub_organization"].choices = [(obj.id, str(obj)) for obj in queryset] + [
+                ("other", "Other (enter your suborganization manually)")
+            ]
+
+    @classmethod
+    def from_database(cls, obj: DomainRequest | Contact | None):
+        """Returns a dict of form field values gotten from `obj`.
+        Overrides RegistrarForm method in order to set sub_organization to 'other'
+        on GETs of the RequestingEntityForm."""
+        if obj is None:
+            return {}
+        # get the domain request as a dict, per usual method
+        domain_request_dict = {name: getattr(obj, name) for name in cls.declared_fields.keys()}  # type: ignore
+
+        # set sub_organization to 'other' if is_requesting_new_suborganization is True
+        if isinstance(obj, DomainRequest) and obj.is_requesting_new_suborganization():
+            domain_request_dict["sub_organization"] = "other"
+
+        return domain_request_dict
 
     def clean_sub_organization(self):
         """On suborganization clean, set the suborganization value to None if the user is requesting
         a custom suborganization (as it doesn't exist yet)"""
-
         # If it's a new suborganization, return None (equivalent to selecting nothing)
         if self.cleaned_data.get("is_requesting_new_suborganization"):
             return None
@@ -94,41 +117,60 @@ def clean_requested_suborganization(self):
         return name
 
     def full_clean(self):
-        """Validation logic to remove the custom suborganization value before clean is triggered.
+        """Validation logic to temporarily remove the custom suborganization value before clean is triggered.
         Without this override, the form will throw an 'invalid option' error."""
-        # Remove the custom other field before cleaning
-        data = self.data.copy() if self.data else None
-
-        # Remove the 'other' value from suborganization if it exists.
-        # This is a special value that tracks if the user is requesting a new suborg.
-        suborganization = self.data.get("portfolio_requesting_entity-sub_organization")
-        if suborganization and "other" in suborganization:
-            data["portfolio_requesting_entity-sub_organization"] = ""
-
-        # Set the modified data back to the form
-        self.data = data
+        # Ensure self.data is not None before proceeding
+        if self.data:
+            # handle case where form has been submitted
+            # Create a copy of the data for manipulation
+            data = self.data.copy()
+
+            # Retrieve sub_organization and store in _original_suborganization
+            suborganization = data.get("portfolio_requesting_entity-sub_organization")
+            self._original_suborganization = suborganization
+            # If the original value was "other", clear it for validation
+            if self._original_suborganization == "other":
+                data["portfolio_requesting_entity-sub_organization"] = ""
+
+            # Set the modified data back to the form
+            self.data = data
+        else:
+            # handle case of a GET
+            suborganization = None
+            if self.initial and "sub_organization" in self.initial:
+                suborganization = self.initial["sub_organization"]
+
+            # Check if is_requesting_new_suborganization is True
+            is_requesting_new_suborganization = False
+            if self.initial and "is_requesting_new_suborganization" in self.initial:
+                # Call the method if it exists
+                is_requesting_new_suborganization = self.initial["is_requesting_new_suborganization"]()
+
+            # Determine if "other" should be set
+            if is_requesting_new_suborganization and suborganization is None:
+                self._original_suborganization = "other"
+            else:
+                self._original_suborganization = suborganization
 
         # Call the parent's full_clean method
         super().full_clean()
 
+        # Restore "other" if there are errors
+        if self.errors:
+            self.data["portfolio_requesting_entity-sub_organization"] = self._original_suborganization
+
     def clean(self):
-        """Custom clean implementation to handle our desired logic flow for suborganization.
-        Given that these fields often rely on eachother, we need to do this in the parent function."""
+        """Custom clean implementation to handle our desired logic flow for suborganization."""
         cleaned_data = super().clean()
 
-        # Do some custom error validation if the requesting entity is a suborg.
-        # Otherwise, just validate as normal.
-        suborganization = self.cleaned_data.get("sub_organization")
-        is_requesting_new_suborganization = self.cleaned_data.get("is_requesting_new_suborganization")
-
-        # Get the value of the yes/no checkbox from RequestingEntityYesNoForm.
-        # Since self.data stores this as a string, we need to convert "True" => True.
+        # Get the cleaned data
+        suborganization = cleaned_data.get("sub_organization")
+        is_requesting_new_suborganization = cleaned_data.get("is_requesting_new_suborganization")
         requesting_entity_is_suborganization = self.data.get(
             "portfolio_requesting_entity-requesting_entity_is_suborganization"
         )
         if requesting_entity_is_suborganization == "True":
             if is_requesting_new_suborganization:
-                # Validate custom suborganization fields
                 if not cleaned_data.get("requested_suborganization") and "requested_suborganization" not in self.errors:
                     self.add_error("requested_suborganization", "Enter the name of your suborganization.")
                 if not cleaned_data.get("suborganization_city"):
@@ -141,6 +183,12 @@ def clean(self):
             elif not suborganization:
                 self.add_error("sub_organization", "Suborganization is required.")
 
+        # If there are errors, restore the "other" value for rendering
+        if self.errors and getattr(self, "_original_suborganization", None) == "other":
+            self.cleaned_data["sub_organization"] = self._original_suborganization
+        elif not self.data and getattr(self, "_original_suborganization", None) == "other":
+            self.cleaned_data["sub_organization"] = self._original_suborganization
+
         return cleaned_data
 
 
@@ -274,7 +322,7 @@ class OrganizationContactForm(RegistrarForm):
         # uncomment to see if modelChoiceField can be an arg later
         required=False,
         queryset=FederalAgency.objects.exclude(agency__in=excluded_agencies),
-        empty_label="--Select--",
+        widget=ComboboxWidget,
     )
     organization_name = forms.CharField(
         label="Organization name",
@@ -294,10 +342,11 @@ class OrganizationContactForm(RegistrarForm):
     )
     state_territory = forms.ChoiceField(
         label="State, territory, or military post",
-        choices=[("", "--Select--")] + DomainRequest.StateTerritoryChoices.choices,
+        choices=DomainRequest.StateTerritoryChoices.choices,
         error_messages={
             "required": ("Select the state, territory, or military post where your organization is located.")
         },
+        widget=ComboboxWidget,
     )
     zipcode = forms.CharField(
         label="Zip code",
diff --git a/src/registrar/forms/portfolio.py b/src/registrar/forms/portfolio.py
index 0a8c4d623..9d6c9ecdf 100644
--- a/src/registrar/forms/portfolio.py
+++ b/src/registrar/forms/portfolio.py
@@ -6,6 +6,7 @@
 from django.core.validators import MaxLengthValidator
 from django.utils.safestring import mark_safe
 
+from registrar.forms.utility.combobox import ComboboxWidget
 from registrar.models import (
     PortfolioInvitation,
     UserPortfolioPermission,
@@ -33,6 +34,15 @@ class PortfolioOrgAddressForm(forms.ModelForm):
             "required": "Enter a 5-digit or 9-digit zip code, like 12345 or 12345-6789.",
         },
     )
+    state_territory = forms.ChoiceField(
+        label="State, territory, or military post",
+        required=True,
+        choices=DomainInformation.StateTerritoryChoices.choices,
+        error_messages={
+            "required": ("Select the state, territory, or military post where your organization is located.")
+        },
+        widget=ComboboxWidget,
+    )
 
     class Meta:
         model = Portfolio
@@ -47,25 +57,12 @@ class Meta:
         error_messages = {
             "address_line1": {"required": "Enter the street address of your organization."},
             "city": {"required": "Enter the city where your organization is located."},
-            "state_territory": {
-                "required": "Select the state, territory, or military post where your organization is located."
-            },
             "zipcode": {"required": "Enter a 5-digit or 9-digit zip code, like 12345 or 12345-6789."},
         }
         widgets = {
-            # We need to set the required attributed for State/territory
-            # because for this fields we are creating an individual
-            # instance of the Select. For the other fields we use the for loop to set
-            # the class's required attribute to true.
             "address_line1": forms.TextInput,
             "address_line2": forms.TextInput,
             "city": forms.TextInput,
-            "state_territory": forms.Select(
-                attrs={
-                    "required": True,
-                },
-                choices=DomainInformation.StateTerritoryChoices.choices,
-            ),
             # "urbanization": forms.TextInput,
         }
 
diff --git a/src/registrar/forms/utility/combobox.py b/src/registrar/forms/utility/combobox.py
new file mode 100644
index 000000000..277aec4f3
--- /dev/null
+++ b/src/registrar/forms/utility/combobox.py
@@ -0,0 +1,5 @@
+from django.forms import Select
+
+
+class ComboboxWidget(Select):
+    template_name = "django/forms/widgets/combobox.html"
diff --git a/src/registrar/templates/django/forms/widgets/combobox.html b/src/registrar/templates/django/forms/widgets/combobox.html
index 7ff31945b..02cd4e35e 100644
--- a/src/registrar/templates/django/forms/widgets/combobox.html
+++ b/src/registrar/templates/django/forms/widgets/combobox.html
@@ -11,6 +11,7 @@
         {{ name }}="{{ value }}"
     {% endif %}
 {% endfor %}
+data-default-value="{% for group_name, group_choices, group_index in widget.optgroups %}{% for option in group_choices %}{% if option.selected %}{{ option.value }}{% endif %}{% endfor %}{% endfor %}"
 >
-    {% include "django/forms/widgets/select.html" %}
+    {% include "django/forms/widgets/select.html" with is_combobox=True %}
 </div>
diff --git a/src/registrar/templates/django/forms/widgets/select.html b/src/registrar/templates/django/forms/widgets/select.html
index cc62eb91d..db6deafe2 100644
--- a/src/registrar/templates/django/forms/widgets/select.html
+++ b/src/registrar/templates/django/forms/widgets/select.html
@@ -3,6 +3,9 @@
     {# hint: spacing in the class string matters #}
     class="usa-select{% if classes %} {{ classes }}{% endif %}"
     {% include "django/forms/widgets/attrs.html" %}
+    {% if is_combobox %}
+      data-default-value="{% for group_name, group_choices, group_index in widget.optgroups %}{% for option in group_choices %}{% if option.selected %}{{ option.value }}{% endif %}{% endfor %}{% endfor %}"
+    {% endif %}
 >
   {% for group, options, index in widget.optgroups %}
     {% if group %}<optgroup label="{{ group }}">{% endif %}
diff --git a/src/registrar/tests/test_views_portfolio.py b/src/registrar/tests/test_views_portfolio.py
index 78a4dae82..e2de3328f 100644
--- a/src/registrar/tests/test_views_portfolio.py
+++ b/src/registrar/tests/test_views_portfolio.py
@@ -2879,7 +2879,7 @@ def test_requesting_entity_page_new_suborg_submission(self):
 
         form["portfolio_requesting_entity-requesting_entity_is_suborganization"] = True
         form["portfolio_requesting_entity-is_requesting_new_suborganization"] = True
-        form["portfolio_requesting_entity-sub_organization"] = ""
+        form["portfolio_requesting_entity-sub_organization"] = "other"
 
         form["portfolio_requesting_entity-requested_suborganization"] = "moon"
         form["portfolio_requesting_entity-suborganization_city"] = "kepler"
@@ -2933,7 +2933,7 @@ def test_requesting_entity_page_organization_submission(self):
 
     @override_flag("organization_feature", active=True)
     @override_flag("organization_requests", active=True)
-    @less_console_noise_decorator
+    # @less_console_noise_decorator
     def test_requesting_entity_page_errors(self):
         """Tests that we get the expected form errors on requesting entity"""
         domain_request = completed_domain_request(user=self.user, portfolio=self.portfolio)
@@ -2942,18 +2942,34 @@ def test_requesting_entity_page_errors(self):
         session_id = self.app.cookies[settings.SESSION_COOKIE_NAME]
         self.app.set_cookie(settings.SESSION_COOKIE_NAME, session_id)
 
+        # For 2 the tests below, it is required to submit a form without submitting a value
+        # for the select/combobox. WebTest will not do this; by default, WebTest will submit
+        # the first choice in a select. So, need to manipulate the form to remove the
+        # particular select/combobox that will not be submitted, and then post the form.
+        form_action = f"/request/{domain_request.pk}/portfolio_requesting_entity/"
+
         # Test missing suborganization selection
         form["portfolio_requesting_entity-requesting_entity_is_suborganization"] = True
-        form["portfolio_requesting_entity-sub_organization"] = ""
-
-        response = form.submit()
+        form["portfolio_requesting_entity-is_requesting_new_suborganization"] = False
+        # remove sub_organization from the form submission
+        form_data = form.submit_fields()
+        form_data = [(key, value) for key, value in form_data if key != "portfolio_requesting_entity-sub_organization"]
+        response = self.app.post(form_action, dict(form_data))
         self.app.set_cookie(settings.SESSION_COOKIE_NAME, session_id)
         self.assertContains(response, "Suborganization is required.", status_code=200)
 
         # Test missing custom suborganization details
+        form["portfolio_requesting_entity-requesting_entity_is_suborganization"] = True
         form["portfolio_requesting_entity-is_requesting_new_suborganization"] = True
-        response = form.submit()
-        self.app.set_cookie(settings.SESSION_COOKIE_NAME, session_id)
+        form["portfolio_requesting_entity-sub_organization"] = "other"
+        # remove suborganization_state_territory from the form submission
+        form_data = form.submit_fields()
+        form_data = [
+            (key, value)
+            for key, value in form_data
+            if key != "portfolio_requesting_entity-suborganization_state_territory"
+        ]
+        response = self.app.post(form_action, dict(form_data))
         self.assertContains(response, "Enter the name of your suborganization.", status_code=200)
         self.assertContains(response, "Enter the city where your suborganization is located.", status_code=200)
         self.assertContains(
diff --git a/src/registrar/views/domain_request.py b/src/registrar/views/domain_request.py
index 9754b0d0c..bff3e5c00 100644
--- a/src/registrar/views/domain_request.py
+++ b/src/registrar/views/domain_request.py
@@ -368,7 +368,6 @@ def get_forms(self, step=None, use_post=False, use_db=False, files=None):
         and from the database if `use_db` is True (provided that record exists).
         An empty form will be provided if neither of those are true.
         """
-
         kwargs = {
             "files": files,
             "prefix": self.steps.current,